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Published in: Malaria Journal 1/2018

Open Access 01-12-2018 | Research

Multiplicity and molecular epidemiology of Plasmodium vivax and Plasmodium falciparum infections in East Africa

Authors: Daibin Zhong, Eugenia Lo, Xiaoming Wang, Delenasaw Yewhalaw, Guofa Zhou, Harrysone E. Atieli, Andrew Githeko, Elizabeth Hemming-Schroeder, Ming-Chieh Lee, Yaw Afrane, Guiyun Yan

Published in: Malaria Journal | Issue 1/2018

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Abstract

Background

Parasite genetic diversity and multiplicity of infection (MOI) affect clinical outcomes, response to drug treatment and naturally-acquired or vaccine-induced immunity. Traditional methods often underestimate the frequency and diversity of multiclonal infections due to technical sensitivity and specificity. Next-generation sequencing techniques provide a novel opportunity to study complexity of parasite populations and molecular epidemiology.

Methods

Symptomatic and asymptomatic Plasmodium vivax samples were collected from health centres/hospitals and schools, respectively, from 2011 to 2015 in Ethiopia. Similarly, both symptomatic and asymptomatic Plasmodium falciparum samples were collected, respectively, from hospitals and schools in 2005 and 2015 in Kenya. Finger-pricked blood samples were collected and dried on filter paper. Long amplicon (> 400 bp) deep sequencing of merozoite surface protein 1 (msp1) gene was conducted to determine multiplicity and molecular epidemiology of P. vivax and P. falciparum infections. The results were compared with those based on short amplicon (117 bp) deep sequencing.

Results

A total of 139 P. vivax and 222 P. falciparum samples were pyro-sequenced for pvmsp1 and pfmsp1, yielding a total of 21 P. vivax and 99 P. falciparum predominant haplotypes. The average MOI for P. vivax and P. falciparum were 2.16 and 2.68, respectively, which were significantly higher than that of microsatellite markers and short amplicon (117 bp) deep sequencing. Multiclonal infections were detected in 62.2% of the samples for P. vivax and 74.8% of the samples for P. falciparum. Four out of the five subjects with recurrent P. vivax malaria were found to be a relapse 44–65 days after clearance of parasites. No difference was observed in MOI among P. vivax patients of different symptoms, ages and genders. Similar patterns were also observed in P. falciparum except for one study site in Kenyan lowland areas with significantly higher MOI.

Conclusions

The study used a novel method to evaluate Plasmodium MOI and molecular epidemiological patterns by long amplicon ultra-deep sequencing. The complexity of infections were similar among age groups, symptoms, genders, transmission settings (spatial heterogeneity), as well as over years (pre- vs. post-scale-up interventions). This study demonstrated that long amplicon deep sequencing is a useful tool to investigate multiplicity and molecular epidemiology of Plasmodium parasite infections.
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Literature
1.
go back to reference WHO. World Malaria Report 2017. Geneva: World Health Organization; 2017. WHO. World Malaria Report 2017. Geneva: World Health Organization; 2017.
2.
4.
go back to reference White MT, Shirreff G, Karl S, Ghani AC, Mueller I. Variation in relapse frequency and the transmission potential of Plasmodium vivax malaria. Proc Biol Sci. 2016;283:20160048.CrossRefPubMedPubMedCentral White MT, Shirreff G, Karl S, Ghani AC, Mueller I. Variation in relapse frequency and the transmission potential of Plasmodium vivax malaria. Proc Biol Sci. 2016;283:20160048.CrossRefPubMedPubMedCentral
5.
go back to reference WHO. World Malaria Report. Geneva: World Health Organization; 2016. WHO. World Malaria Report. Geneva: World Health Organization; 2016.
6.
go back to reference Mideo N, Bailey JA, Hathaway NJ, Ngasala B, Saunders DL, Lon C, et al. A deep sequencing tool for partitioning clearance rates following antimalarial treatment in polyclonal infections. Evol Med Public Health. 2016;2016:21–36.CrossRefPubMedPubMedCentral Mideo N, Bailey JA, Hathaway NJ, Ngasala B, Saunders DL, Lon C, et al. A deep sequencing tool for partitioning clearance rates following antimalarial treatment in polyclonal infections. Evol Med Public Health. 2016;2016:21–36.CrossRefPubMedPubMedCentral
7.
go back to reference Ngondi JM, Ishengoma DS, Doctor SM, Thwai KL, Keeler C, Mkude S, et al. Surveillance for sulfadoxine-pyrimethamine resistant malaria parasites in the Lake and Southern Zones, Tanzania, using pooling and next-generation sequencing. Malar J. 2017;16:236.CrossRefPubMedPubMedCentral Ngondi JM, Ishengoma DS, Doctor SM, Thwai KL, Keeler C, Mkude S, et al. Surveillance for sulfadoxine-pyrimethamine resistant malaria parasites in the Lake and Southern Zones, Tanzania, using pooling and next-generation sequencing. Malar J. 2017;16:236.CrossRefPubMedPubMedCentral
8.
go back to reference Rao PN, Uplekar S, Kayal S, Mallick PK, Bandyopadhyay N, Kale S, et al. A method for amplicon deep sequencing of drug resistance genes in Plasmodium falciparum clinical isolates from India. J Clin Microbiol. 2016;54:1500–11.CrossRefPubMedPubMedCentral Rao PN, Uplekar S, Kayal S, Mallick PK, Bandyopadhyay N, Kale S, et al. A method for amplicon deep sequencing of drug resistance genes in Plasmodium falciparum clinical isolates from India. J Clin Microbiol. 2016;54:1500–11.CrossRefPubMedPubMedCentral
9.
go back to reference Tusting LS, Bousema T, Smith DL, Drakeley C. Measuring changes in Plasmodium falciparum transmission: precision, accuracy and costs of metrics. Adv Parasitol. 2014;84:151–208.CrossRefPubMedPubMedCentral Tusting LS, Bousema T, Smith DL, Drakeley C. Measuring changes in Plasmodium falciparum transmission: precision, accuracy and costs of metrics. Adv Parasitol. 2014;84:151–208.CrossRefPubMedPubMedCentral
10.
go back to reference Juliano JJ, Parobek CM, Brazeau NF, Ngasala B, Randrianarivelojosia M, Lon C, et al. Pooled amplicon deep sequencing of candidate Plasmodium falciparum transmission-blocking vaccine antigens. Am J Trop Med Hyg. 2016;94:143–6.CrossRefPubMedPubMedCentral Juliano JJ, Parobek CM, Brazeau NF, Ngasala B, Randrianarivelojosia M, Lon C, et al. Pooled amplicon deep sequencing of candidate Plasmodium falciparum transmission-blocking vaccine antigens. Am J Trop Med Hyg. 2016;94:143–6.CrossRefPubMedPubMedCentral
11.
go back to reference Parobek CM, Bailey JA, Hathaway NJ, Socheat D, Rogers WO, Juliano JJ. Differing patterns of selection and geospatial genetic diversity within two leading Plasmodium vivax candidate vaccine antigens. PLoS Negl Trop Dis. 2014;8:e2796.CrossRefPubMedPubMedCentral Parobek CM, Bailey JA, Hathaway NJ, Socheat D, Rogers WO, Juliano JJ. Differing patterns of selection and geospatial genetic diversity within two leading Plasmodium vivax candidate vaccine antigens. PLoS Negl Trop Dis. 2014;8:e2796.CrossRefPubMedPubMedCentral
12.
go back to reference Juliano JJ, Porter K, Mwapasa V, Sem R, Rogers WO, Ariey F, et al. Exposing malaria in-host diversity and estimating population diversity by capture-recapture using massively parallel pyrosequencing. Proc Natl Acad Sci USA. 2010;107:20138–43.CrossRefPubMedPubMedCentral Juliano JJ, Porter K, Mwapasa V, Sem R, Rogers WO, Ariey F, et al. Exposing malaria in-host diversity and estimating population diversity by capture-recapture using massively parallel pyrosequencing. Proc Natl Acad Sci USA. 2010;107:20138–43.CrossRefPubMedPubMedCentral
13.
go back to reference de Souza AM, de Araujo FC, Fontes CJ, Carvalho LH, de Brito CF, de Sousa TN. Multiple-clone infections of Plasmodium vivax: definition of a panel of markers for molecular epidemiology. Malar J. 2015;14:330.CrossRefPubMedPubMedCentral de Souza AM, de Araujo FC, Fontes CJ, Carvalho LH, de Brito CF, de Sousa TN. Multiple-clone infections of Plasmodium vivax: definition of a panel of markers for molecular epidemiology. Malar J. 2015;14:330.CrossRefPubMedPubMedCentral
14.
go back to reference Lin JT, Juliano JJ, Kharabora O, Sem R, Lin FC, Muth S, et al. Individual Plasmodium vivax msp1 variants within polyclonal P. vivax infections display different propensities for relapse. J Clin Microbiol. 2012;50:1449–51.CrossRefPubMedPubMedCentral Lin JT, Juliano JJ, Kharabora O, Sem R, Lin FC, Muth S, et al. Individual Plasmodium vivax msp1 variants within polyclonal P. vivax infections display different propensities for relapse. J Clin Microbiol. 2012;50:1449–51.CrossRefPubMedPubMedCentral
15.
go back to reference Lin JT, Hathaway NJ, Saunders DL, Lon C, Balasubramanian S, Kharabora O, et al. Using amplicon deep sequencing to detect genetic signatures of Plasmodium vivax relapse. J Infect Dis. 2015;212:999–1008.CrossRefPubMedPubMedCentral Lin JT, Hathaway NJ, Saunders DL, Lon C, Balasubramanian S, Kharabora O, et al. Using amplicon deep sequencing to detect genetic signatures of Plasmodium vivax relapse. J Infect Dis. 2015;212:999–1008.CrossRefPubMedPubMedCentral
16.
go back to reference Hussain MM, Sohail M, Kumar R, Branch OH, Adak T, Raziuddin M. Genetic diversity in merozoite surface protein-1 and 2 among Plasmodium falciparum isolates from malarious districts of tribal dominant state of Jharkhand, India. Ann Trop Med Parasitol. 2011;105:579–92.CrossRefPubMedPubMedCentral Hussain MM, Sohail M, Kumar R, Branch OH, Adak T, Raziuddin M. Genetic diversity in merozoite surface protein-1 and 2 among Plasmodium falciparum isolates from malarious districts of tribal dominant state of Jharkhand, India. Ann Trop Med Parasitol. 2011;105:579–92.CrossRefPubMedPubMedCentral
17.
go back to reference Congpuong K, Sukaram R, Prompan Y, Dornae A. Genetic diversity of the msp-1, msp-2, and glurp genes of Plasmodium falciparum isolates along the Thai–Myanmar borders. Asian Pac J Trop Biomed. 2014;4:598–602.CrossRefPubMedPubMedCentral Congpuong K, Sukaram R, Prompan Y, Dornae A. Genetic diversity of the msp-1, msp-2, and glurp genes of Plasmodium falciparum isolates along the Thai–Myanmar borders. Asian Pac J Trop Biomed. 2014;4:598–602.CrossRefPubMedPubMedCentral
18.
go back to reference Khaminsou N, Kritpetcharat O, Daduang J, Charerntanyarak L, Kritpetcharat P. Genetic analysis of the merozoite surface protein-1 block 2 allelic types in Plasmodium falciparum clinical isolates from Lao PDR. Malar J. 2011;10:371.CrossRefPubMedPubMedCentral Khaminsou N, Kritpetcharat O, Daduang J, Charerntanyarak L, Kritpetcharat P. Genetic analysis of the merozoite surface protein-1 block 2 allelic types in Plasmodium falciparum clinical isolates from Lao PDR. Malar J. 2011;10:371.CrossRefPubMedPubMedCentral
19.
go back to reference Messerli C, Hofmann NE, Beck H-P, Felger I. Critical evaluation of molecular monitoring in malaria drug efficacy trials and pitfalls of length-polymorphic markers. Antimicrob Agents Chemother. 2017;61:e01500–16.CrossRefPubMed Messerli C, Hofmann NE, Beck H-P, Felger I. Critical evaluation of molecular monitoring in malaria drug efficacy trials and pitfalls of length-polymorphic markers. Antimicrob Agents Chemother. 2017;61:e01500–16.CrossRefPubMed
20.
go back to reference Bouyou-Akotet MK, M’Bondoukwe NP, Mawili-Mboumba DP. Genetic polymorphism of merozoite surface protein-1 in Plasmodium falciparum isolates from patients with mild to severe malaria in Libreville, Gabon. Parasite. 2015;22:12.CrossRefPubMedPubMedCentral Bouyou-Akotet MK, M’Bondoukwe NP, Mawili-Mboumba DP. Genetic polymorphism of merozoite surface protein-1 in Plasmodium falciparum isolates from patients with mild to severe malaria in Libreville, Gabon. Parasite. 2015;22:12.CrossRefPubMedPubMedCentral
21.
22.
go back to reference Lalremruata A, Jeyaraj S, Engleitner T, Joanny F, Lang A, Belard S, et al. Species and genotype diversity of Plasmodium in malaria patients from Gabon analysed by next generation sequencing. Malar J. 2017;16:398.CrossRefPubMedPubMedCentral Lalremruata A, Jeyaraj S, Engleitner T, Joanny F, Lang A, Belard S, et al. Species and genotype diversity of Plasmodium in malaria patients from Gabon analysed by next generation sequencing. Malar J. 2017;16:398.CrossRefPubMedPubMedCentral
23.
go back to reference Lerch A, Koepfli C, Hofmann N, Messerli C, Wilcox S, Kattenberg JH, et al. Development of amplicon deep sequencing markers and data analysis pipeline for genotyping multi-clonal malaria infections. BMC Genomics. 2017;18:864.CrossRefPubMedPubMedCentral Lerch A, Koepfli C, Hofmann N, Messerli C, Wilcox S, Kattenberg JH, et al. Development of amplicon deep sequencing markers and data analysis pipeline for genotyping multi-clonal malaria infections. BMC Genomics. 2017;18:864.CrossRefPubMedPubMedCentral
24.
go back to reference Gilson PR, Nebl T, Vukcevic D, Moritz RL, Sargeant T, Speed TP, et al. Identification and stoichiometry of glycosylphosphatidylinositol-anchored membrane proteins of the human malaria parasite Plasmodium falciparum. Mol Cell Proteomics. 2006;5:1286–99.CrossRefPubMed Gilson PR, Nebl T, Vukcevic D, Moritz RL, Sargeant T, Speed TP, et al. Identification and stoichiometry of glycosylphosphatidylinositol-anchored membrane proteins of the human malaria parasite Plasmodium falciparum. Mol Cell Proteomics. 2006;5:1286–99.CrossRefPubMed
25.
go back to reference Lin CS, Uboldi AD, Epp C, Bujard H, Tsuboi T, Czabotar PE, et al. Multiple Plasmodium falciparum merozoite surface protein 1 complexes mediate merozoite binding to human erythrocytes. J Bio Chem. 2016;291:7703–15.CrossRef Lin CS, Uboldi AD, Epp C, Bujard H, Tsuboi T, Czabotar PE, et al. Multiple Plasmodium falciparum merozoite surface protein 1 complexes mediate merozoite binding to human erythrocytes. J Bio Chem. 2016;291:7703–15.CrossRef
26.
go back to reference Baldwin MR, Li X, Hanada T, Liu SC, Chishti AH. Merozoite surface protein 1 recognition of host glycophorin A mediates malaria parasite invasion of red blood cells. Blood. 2015;125:2704–11.CrossRefPubMedPubMedCentral Baldwin MR, Li X, Hanada T, Liu SC, Chishti AH. Merozoite surface protein 1 recognition of host glycophorin A mediates malaria parasite invasion of red blood cells. Blood. 2015;125:2704–11.CrossRefPubMedPubMedCentral
27.
go back to reference Tanabe K, Mackay M, Goman M, Scaife JG. Allelic dimorphism in a surface antigen gene of the malaria parasite Plasmodium falciparum. J Mol Biol. 1987;195:273–87.CrossRefPubMed Tanabe K, Mackay M, Goman M, Scaife JG. Allelic dimorphism in a surface antigen gene of the malaria parasite Plasmodium falciparum. J Mol Biol. 1987;195:273–87.CrossRefPubMed
28.
go back to reference del Portillo HA, Longacre S, Khouri E, David PH. Primary structure of the merozoite surface antigen 1 of Plasmodium vivax reveals sequences conserved between different Plasmodium species. Proc Natl Acad Sci USA. 1991;88:4030–4.CrossRefPubMedPubMedCentral del Portillo HA, Longacre S, Khouri E, David PH. Primary structure of the merozoite surface antigen 1 of Plasmodium vivax reveals sequences conserved between different Plasmodium species. Proc Natl Acad Sci USA. 1991;88:4030–4.CrossRefPubMedPubMedCentral
29.
go back to reference Alemu A, Abebe G, Tsegaye W, Golassa L. Climatic variables and malaria transmission dynamics in Jimma town, South West Ethiopia. Parasit Vectors. 2011;4:30.CrossRefPubMedPubMedCentral Alemu A, Abebe G, Tsegaye W, Golassa L. Climatic variables and malaria transmission dynamics in Jimma town, South West Ethiopia. Parasit Vectors. 2011;4:30.CrossRefPubMedPubMedCentral
30.
go back to reference Demissie F, Kebede A, Shimels T, Beyene P. Assessment of public health implication of malaria-geohelminth co-infection with an emphasis on hookworm-malaria anemia among suspected malaria patients in asendabo, southwest Ethiopia. Ethiop Med J. 2009;47:153–8.PubMed Demissie F, Kebede A, Shimels T, Beyene P. Assessment of public health implication of malaria-geohelminth co-infection with an emphasis on hookworm-malaria anemia among suspected malaria patients in asendabo, southwest Ethiopia. Ethiop Med J. 2009;47:153–8.PubMed
31.
go back to reference Zhou G, Yewhalaw D, Lo E, Zhong D, Wang X, Degefa T, et al. Analysis of asymptomatic and clinical malaria in urban and suburban settings of southwestern Ethiopia in the context of sustaining malaria control and approaching elimination. Malar J. 2016;15:250.CrossRefPubMedPubMedCentral Zhou G, Yewhalaw D, Lo E, Zhong D, Wang X, Degefa T, et al. Analysis of asymptomatic and clinical malaria in urban and suburban settings of southwestern Ethiopia in the context of sustaining malaria control and approaching elimination. Malar J. 2016;15:250.CrossRefPubMedPubMedCentral
32.
33.
go back to reference Otsyula GM, Andrew G, Guofa Z, Emmanuel M, Noboru M, Guiyun Y. Plasmodium falciparum spatial analysis, Western Kenya highlands. Emerg Infect Dis. 2005;11:1571.CrossRef Otsyula GM, Andrew G, Guofa Z, Emmanuel M, Noboru M, Guiyun Y. Plasmodium falciparum spatial analysis, Western Kenya highlands. Emerg Infect Dis. 2005;11:1571.CrossRef
34.
go back to reference Lo E, Nguyen K, Nguyen J, Hemming-Schroeder E, Xu J, Etemesi H, et al. Plasmodium malariae prevalence and csp gene diversity, Kenya, 2014 and 2015. Emerg Infect Dis. 2017;23:601–10.CrossRefPubMedPubMedCentral Lo E, Nguyen K, Nguyen J, Hemming-Schroeder E, Xu J, Etemesi H, et al. Plasmodium malariae prevalence and csp gene diversity, Kenya, 2014 and 2015. Emerg Infect Dis. 2017;23:601–10.CrossRefPubMedPubMedCentral
35.
go back to reference National Malaria Control Programme (NMCP), Kenya National Bureau of Statistics (KNBS). ICF International: Kenya malaria indicator survey 2015. Maryland: NMCP, KNBS, and ICF International; 2016. National Malaria Control Programme (NMCP), Kenya National Bureau of Statistics (KNBS). ICF International: Kenya malaria indicator survey 2015. Maryland: NMCP, KNBS, and ICF International; 2016.
36.
go back to reference Zhou G, Afrane YA, Vardo-Zalik AM, Atieli H, Zhong D, Wamae P, et al. Changing patterns of malaria epidemiology between 2002 and 2010 in western Kenya: the fall and rise of malaria. PLoS ONE. 2011;6:e20318.CrossRefPubMedPubMedCentral Zhou G, Afrane YA, Vardo-Zalik AM, Atieli H, Zhong D, Wamae P, et al. Changing patterns of malaria epidemiology between 2002 and 2010 in western Kenya: the fall and rise of malaria. PLoS ONE. 2011;6:e20318.CrossRefPubMedPubMedCentral
37.
go back to reference Zhou G, Lee MC, Githeko AK, Atieli HE, Yan G. Insecticide-treated net campaign and malaria transmission in western Kenya: 2003-2015. Front Public Health. 2016;4:153.CrossRefPubMedPubMedCentral Zhou G, Lee MC, Githeko AK, Atieli HE, Yan G. Insecticide-treated net campaign and malaria transmission in western Kenya: 2003-2015. Front Public Health. 2016;4:153.CrossRefPubMedPubMedCentral
38.
go back to reference Lo E, Zhou G, Oo W, Afrane Y, Githeko A, Yan G. Low parasitemia in submicroscopic infections significantly impacts malaria diagnostic sensitivity in the highlands of Western Kenya. PLoS ONE. 2015;10:e0121763.CrossRefPubMedPubMedCentral Lo E, Zhou G, Oo W, Afrane Y, Githeko A, Yan G. Low parasitemia in submicroscopic infections significantly impacts malaria diagnostic sensitivity in the highlands of Western Kenya. PLoS ONE. 2015;10:e0121763.CrossRefPubMedPubMedCentral
39.
go back to reference Lo E, Hemming-Schroeder E, Yewhalaw D, Nguyen J, Kebede E, Zemene E, et al. Transmission dynamics of co-endemic Plasmodium vivax and P. falciparum in Ethiopia and prevalence of antimalarial resistant genotypes. PLoS Negl Trop Dis. 2017;11:e0005806.CrossRefPubMedPubMedCentral Lo E, Hemming-Schroeder E, Yewhalaw D, Nguyen J, Kebede E, Zemene E, et al. Transmission dynamics of co-endemic Plasmodium vivax and P. falciparum in Ethiopia and prevalence of antimalarial resistant genotypes. PLoS Negl Trop Dis. 2017;11:e0005806.CrossRefPubMedPubMedCentral
40.
go back to reference Zhong D, Afrane Y, Githeko A, Cui L, Menge DM, Yan G. Molecular epidemiology of drug-resistant malaria in western Kenya highlands. BMC Infect Dis. 2008;8:105.CrossRefPubMedPubMedCentral Zhong D, Afrane Y, Githeko A, Cui L, Menge DM, Yan G. Molecular epidemiology of drug-resistant malaria in western Kenya highlands. BMC Infect Dis. 2008;8:105.CrossRefPubMedPubMedCentral
41.
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.PubMed 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.PubMed
42.
go back to reference Bereczky S, Martensson A, Gil JP, Farnert A. Short report: rapid DNA extraction from archive blood spots on filter paper for genotyping of Plasmodium falciparum. Am J Trop Med Hyg. 2005;72:249–51.PubMed Bereczky S, Martensson A, Gil JP, Farnert A. Short report: rapid DNA extraction from archive blood spots on filter paper for genotyping of Plasmodium falciparum. Am J Trop Med Hyg. 2005;72:249–51.PubMed
43.
go back to reference Snounou G, Viriyakosol S, Zhu XP, Jarra W, Pinheiro L, do Rosario VE, et al. High sensitivity of detection of human malaria parasites by the use of nested polymerase chain reaction. Mol Biochem Parasitol. 1993;61:315–20.CrossRefPubMed Snounou G, Viriyakosol S, Zhu XP, Jarra W, Pinheiro L, do Rosario VE, et al. High sensitivity of detection of human malaria parasites by the use of nested polymerase chain reaction. Mol Biochem Parasitol. 1993;61:315–20.CrossRefPubMed
44.
go back to reference Singh B, Bobogare A, Cox-Singh J, Snounou G, Abdullah MS, Rahman HA. A genus- and species-specific nested polymerase chain reaction malaria detection assay for epidemiologic studies. Am J Trop Med Hyg. 1999;60:687–92.CrossRefPubMed Singh B, Bobogare A, Cox-Singh J, Snounou G, Abdullah MS, Rahman HA. A genus- and species-specific nested polymerase chain reaction malaria detection assay for epidemiologic studies. Am J Trop Med Hyg. 1999;60:687–92.CrossRefPubMed
45.
go back to reference Colwell RK, Elsensohn JE. EstimateS turns 20: statistical estimation of species richness and shared species from samples, with non-parametric extrapolation. Ecography. 2014;37:609–13.CrossRef Colwell RK, Elsensohn JE. EstimateS turns 20: statistical estimation of species richness and shared species from samples, with non-parametric extrapolation. Ecography. 2014;37:609–13.CrossRef
46.
go back to reference Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013;30:772–80.CrossRefPubMedPubMedCentral Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013;30:772–80.CrossRefPubMedPubMedCentral
47.
go back to reference Hall TA. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser. 1999;41:95–8. Hall TA. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser. 1999;41:95–8.
48.
go back to reference Librado P, Rozas J. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics. 2009;25:1451–2.CrossRefPubMed Librado P, Rozas J. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics. 2009;25:1451–2.CrossRefPubMed
49.
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.CrossRefPubMed 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.CrossRefPubMed
50.
go back to reference Peakall R, Smouse PE. GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research–an update. Bioinformatics. 2012;28:2537–9.CrossRefPubMedPubMedCentral Peakall R, Smouse PE. GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research–an update. Bioinformatics. 2012;28:2537–9.CrossRefPubMedPubMedCentral
51.
go back to reference Kumar S, Stecher G, Tamura K. MEGA7: molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Mol Biol Evol. 2016;33:1870–4.CrossRefPubMed Kumar S, Stecher G, Tamura K. MEGA7: molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Mol Biol Evol. 2016;33:1870–4.CrossRefPubMed
52.
go back to reference Letunic I, Bork P. Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res. 2016;44:W242–5.CrossRefPubMedPubMedCentral Letunic I, Bork P. Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res. 2016;44:W242–5.CrossRefPubMedPubMedCentral
53.
go back to reference Leigh JW, Bryant D. popart: full-feature software for haplotype network construction. Methods Ecol Evol. 2015;6:1110–6.CrossRef Leigh JW, Bryant D. popart: full-feature software for haplotype network construction. Methods Ecol Evol. 2015;6:1110–6.CrossRef
54.
go back to reference Hathaway NJ, Parobek CM, Juliano JJ, Bailey JA. SeekDeep: single-base resolution de novo clustering for amplicon deep sequencing. Nucleic Acids Res. 2018;46:e21.CrossRefPubMed Hathaway NJ, Parobek CM, Juliano JJ, Bailey JA. SeekDeep: single-base resolution de novo clustering for amplicon deep sequencing. Nucleic Acids Res. 2018;46:e21.CrossRefPubMed
55.
go back to reference Mayor A, Saute F, Aponte JJ, Almeda J, Gomez-Olive FX, Dgedge M, et al. Plasmodium falciparum multiple infections in Mozambique, its relation to other malariological indices and to prospective risk of malaria morbidity. Trop Med Int Health. 2003;8:3–11.CrossRefPubMed Mayor A, Saute F, Aponte JJ, Almeda J, Gomez-Olive FX, Dgedge M, et al. Plasmodium falciparum multiple infections in Mozambique, its relation to other malariological indices and to prospective risk of malaria morbidity. Trop Med Int Health. 2003;8:3–11.CrossRefPubMed
56.
go back to reference Engelbrecht F, Tögel E, Beck H-P, Enwezor F, Oettli A, Felger I. Analysis of Plasmodium falciparum infections in a village community in Northern Nigeria: determination of msp2 genotypes and parasite-specific IgG responses. Acta Trop. 2000;74:63–71.CrossRefPubMed Engelbrecht F, Tögel E, Beck H-P, Enwezor F, Oettli A, Felger I. Analysis of Plasmodium falciparum infections in a village community in Northern Nigeria: determination of msp2 genotypes and parasite-specific IgG responses. Acta Trop. 2000;74:63–71.CrossRefPubMed
57.
go back to reference Nguyen HV, van den Eede P, van Overmeir C, Thang ND, Hung LX, D’Alessandro U, et al. Marked age-dependent prevalence of symptomatic and patent infections and complexity of distribution of human Plasmodium species in central Vietnam. Am J Trop Med Hyg. 2012;87:989–95.CrossRefPubMedPubMedCentral Nguyen HV, van den Eede P, van Overmeir C, Thang ND, Hung LX, D’Alessandro U, et al. Marked age-dependent prevalence of symptomatic and patent infections and complexity of distribution of human Plasmodium species in central Vietnam. Am J Trop Med Hyg. 2012;87:989–95.CrossRefPubMedPubMedCentral
58.
go back to reference Tukwasibwe S, Mugenyi L, Mbogo GW, Nankoberanyi S, Maiteki-Sebuguzi C, Joloba ML, et al. Differential prevalence of transporter polymorphisms in symptomatic and asymptomatic falciparum malaria infections in uganda. J Infect Dis. 2014;210:154–7.CrossRefPubMedPubMedCentral Tukwasibwe S, Mugenyi L, Mbogo GW, Nankoberanyi S, Maiteki-Sebuguzi C, Joloba ML, et al. Differential prevalence of transporter polymorphisms in symptomatic and asymptomatic falciparum malaria infections in uganda. J Infect Dis. 2014;210:154–7.CrossRefPubMedPubMedCentral
59.
go back to reference Waltmann A, Darcy AW, Harris I, Koepfli C, Lodo J, Vahi V, et al. High rates of asymptomatic, sub-microscopic Plasmodium vivax infection and disappearing Plasmodium falciparum malaria in an area of low transmission in Solomon Islands. PLoS Negl Trop Dis. 2015;9:e0003758.CrossRefPubMedPubMedCentral Waltmann A, Darcy AW, Harris I, Koepfli C, Lodo J, Vahi V, et al. High rates of asymptomatic, sub-microscopic Plasmodium vivax infection and disappearing Plasmodium falciparum malaria in an area of low transmission in Solomon Islands. PLoS Negl Trop Dis. 2015;9:e0003758.CrossRefPubMedPubMedCentral
60.
go back to reference Pacheco MA, Lopez-Perez M, Vallejo AF, Herrera S, Arevalo-Herrera M, Escalante AA. Multiplicity of infection and disease severity in Plasmodium vivax. PLoS Negl Trop Dis. 2016;10:e0004355.CrossRefPubMedPubMedCentral Pacheco MA, Lopez-Perez M, Vallejo AF, Herrera S, Arevalo-Herrera M, Escalante AA. Multiplicity of infection and disease severity in Plasmodium vivax. PLoS Negl Trop Dis. 2016;10:e0004355.CrossRefPubMedPubMedCentral
61.
go back to reference Beck S, Mockenhaupt FP, Bienzle U, Eggelte TA, Thompson WN, Stark K. Multiplicity of Plasmodium falciparum infection in pregnancy. Am J Trop Med Hyg. 2001;65:631–6.CrossRefPubMed Beck S, Mockenhaupt FP, Bienzle U, Eggelte TA, Thompson WN, Stark K. Multiplicity of Plasmodium falciparum infection in pregnancy. Am J Trop Med Hyg. 2001;65:631–6.CrossRefPubMed
62.
go back to reference Kiwuwa MS, Ribacke U, Moll K, Byarugaba J, Lundblom K, Farnert 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.CrossRefPubMedPubMedCentral Kiwuwa MS, Ribacke U, Moll K, Byarugaba J, Lundblom K, Farnert 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.CrossRefPubMedPubMedCentral
63.
go back to reference Kun JF, Schmidt-Ott RJ, Lehman LG, Lell B, Luckner D, Greve B, et al. Merozoite surface antigen 1 and 2 genotypes and rosetting of Plasmodium falciparum in severe and mild malaria in Lambarene, Gabon. Trans R Soc Trop Med Hyg. 1998;92:110–4.CrossRefPubMed Kun JF, Schmidt-Ott RJ, Lehman LG, Lell B, Luckner D, Greve B, et al. Merozoite surface antigen 1 and 2 genotypes and rosetting of Plasmodium falciparum in severe and mild malaria in Lambarene, Gabon. Trans R Soc Trop Med Hyg. 1998;92:110–4.CrossRefPubMed
64.
go back to reference Nicastri E, Paglia MG, Severini C, Ghirga P, Bevilacqua N. Disease severity, host characteristics and Plasmodium falciparum multiple infections in malaria affected travellers returning from Africa. Travel Med Infect Dis. 2007;5:405–6.CrossRef Nicastri E, Paglia MG, Severini C, Ghirga P, Bevilacqua N. Disease severity, host characteristics and Plasmodium falciparum multiple infections in malaria affected travellers returning from Africa. Travel Med Infect Dis. 2007;5:405–6.CrossRef
65.
go back to reference Nicastri E, Paglia MG, Severini C, Ghirga P, Bevilacqua N, Narciso P. Plasmodium falciparum multiple infections, disease severity and host characteristics in malaria affected travellers returning from Africa. Travel Med Infect Dis. 2008;6:205–9.CrossRefPubMed Nicastri E, Paglia MG, Severini C, Ghirga P, Bevilacqua N, Narciso P. Plasmodium falciparum multiple infections, disease severity and host characteristics in malaria affected travellers returning from Africa. Travel Med Infect Dis. 2008;6:205–9.CrossRefPubMed
66.
go back to reference Pava Z, Handayuni I, Trianty L, Utami RAS, Tirta YK, Puspitasari AM, et al. Passively versus actively detected malaria: similar genetic diversity but different complexity of infection. Am J Trop Med Hyg. 2017;97:1788–96.CrossRefPubMedPubMedCentral Pava Z, Handayuni I, Trianty L, Utami RAS, Tirta YK, Puspitasari AM, et al. Passively versus actively detected malaria: similar genetic diversity but different complexity of infection. Am J Trop Med Hyg. 2017;97:1788–96.CrossRefPubMedPubMedCentral
67.
go back to reference Ranjit MR, Das A, Das BP, Das BN, Dash BP, Chhotray GP. Distribution of Plasmodium falciparum genotypes in clinically mild and severe malaria cases in Orissa, India. Trans R Soc Trop Med Hyg. 2005;99:389–95.CrossRefPubMed Ranjit MR, Das A, Das BP, Das BN, Dash BP, Chhotray GP. Distribution of Plasmodium falciparum genotypes in clinically mild and severe malaria cases in Orissa, India. Trans R Soc Trop Med Hyg. 2005;99:389–95.CrossRefPubMed
68.
go back to reference Rout R, Mohapatra BN, Kar SK, Ranjit M. Genetic complexity and transmissibility of Plasmodium falciparum parasites causing severe malaria in central-east coast India. Trop Biomed. 2009;26:165–72.PubMed Rout R, Mohapatra BN, Kar SK, Ranjit M. Genetic complexity and transmissibility of Plasmodium falciparum parasites causing severe malaria in central-east coast India. Trop Biomed. 2009;26:165–72.PubMed
69.
go back to reference Conway DJ, Greenwood BM, McBride JS. The epidemiology of multiple-clone Plasmodium falciparum infections in Gambian patients. Parasitology. 2009;103:1–5.CrossRef Conway DJ, Greenwood BM, McBride JS. The epidemiology of multiple-clone Plasmodium falciparum infections in Gambian patients. Parasitology. 2009;103:1–5.CrossRef
70.
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.CrossRefPubMed 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.CrossRefPubMed
71.
go back to reference Mara SE, Silué KD, Raso G, N’Guetta SP, N’Goran EK, Tanner M, et al. Genetic diversity of Plasmodium falciparum among school-aged children from the Man region, western Côte d’Ivoire. Malar J. 2013;2:419.CrossRef Mara SE, Silué KD, Raso G, N’Guetta SP, N’Goran EK, Tanner M, et al. Genetic diversity of Plasmodium falciparum among school-aged children from the Man region, western Côte d’Ivoire. Malar J. 2013;2:419.CrossRef
72.
go back to reference Al-Yaman F, Genton B, Reeder JC, Anders RF, Smith T, Alpers MP. Reduced risk of clinical malaria in children infected with multiple clones of Plasmodium falciparum in a highly endemic area: a prospective community study. Trans R Soc Trop Med Hyg. 1997;91:602–5.CrossRefPubMed Al-Yaman F, Genton B, Reeder JC, Anders RF, Smith T, Alpers MP. Reduced risk of clinical malaria in children infected with multiple clones of Plasmodium falciparum in a highly endemic area: a prospective community study. Trans R Soc Trop Med Hyg. 1997;91:602–5.CrossRefPubMed
73.
go back to reference Bereczky S, Liljander A, Rooth I, Faraja L, Granath F, Montgomery SM, et al. Multiclonal asymptomatic Plasmodium falciparum infections predict a reduced risk of malaria disease in a Tanzanian population. Microbes Infect. 2007;9:103–10.CrossRefPubMed Bereczky S, Liljander A, Rooth I, Faraja L, Granath F, Montgomery SM, et al. Multiclonal asymptomatic Plasmodium falciparum infections predict a reduced risk of malaria disease in a Tanzanian population. Microbes Infect. 2007;9:103–10.CrossRefPubMed
74.
go back to reference Nielsen MA, Staalsoe T, Kurtzhals JA, Goka BQ, Dodoo D, Alifrangis M, et al. Plasmodium falciparum variant surface antigen expression varies between isolates causing severe and nonsevere malaria and is modified by acquired immunity. J Immunol. 2002;168:3444–50.CrossRefPubMed Nielsen MA, Staalsoe T, Kurtzhals JA, Goka BQ, Dodoo D, Alifrangis M, et al. Plasmodium falciparum variant surface antigen expression varies between isolates causing severe and nonsevere malaria and is modified by acquired immunity. J Immunol. 2002;168:3444–50.CrossRefPubMed
75.
go back to reference Amodu OK, Oyedeji SI, Ntoumi F, Orimadegun AE, Gbadegesin RA, Olumese PE, et al. Complexity of the msp2 locus and the severity of childhood malaria, in south-western Nigeria. Ann Trop Med Parasitol. 2008;102:95–102.CrossRefPubMed Amodu OK, Oyedeji SI, Ntoumi F, Orimadegun AE, Gbadegesin RA, Olumese PE, et al. Complexity of the msp2 locus and the severity of childhood malaria, in south-western Nigeria. Ann Trop Med Parasitol. 2008;102:95–102.CrossRefPubMed
76.
go back to reference Noviyanti R, Coutrier F, Utami RA, Trimarsanto H, Tirta YK, Trianty L, et al. Contrasting transmission dynamics of co-endemic Plasmodium vivax and P. falciparum: implications for malaria control and elimination. PLoS Negl Trop Dis. 2015;9:e0003739.CrossRefPubMedPubMedCentral Noviyanti R, Coutrier F, Utami RA, Trimarsanto H, Tirta YK, Trianty L, et al. Contrasting transmission dynamics of co-endemic Plasmodium vivax and P. falciparum: implications for malaria control and elimination. PLoS Negl Trop Dis. 2015;9:e0003739.CrossRefPubMedPubMedCentral
77.
go back to reference Fola AA, Harrison GLA, Hazairin MH, Barnadas C, Hetzel MW, Iga J, et al. Higher complexity of infection and genetic diversity of Plasmodium vivax than Plasmodium falciparum across all malaria transmission zones of papua new guinea. Am J Trop Med Hyg. 2017;96:630–41.PubMedPubMedCentral Fola AA, Harrison GLA, Hazairin MH, Barnadas C, Hetzel MW, Iga J, et al. Higher complexity of infection and genetic diversity of Plasmodium vivax than Plasmodium falciparum across all malaria transmission zones of papua new guinea. Am J Trop Med Hyg. 2017;96:630–41.PubMedPubMedCentral
78.
go back to reference Getachew S, To S, Trimarsanto H, Thriemer K, Clark TG, Petros B, et al. Variation in complexity of infection and transmission stability between neighbouring populations of Plasmodium vivax in southern Ethiopia. PLoS ONE. 2015;10:e0140780.CrossRefPubMedPubMedCentral Getachew S, To S, Trimarsanto H, Thriemer K, Clark TG, Petros B, et al. Variation in complexity of infection and transmission stability between neighbouring populations of Plasmodium vivax in southern Ethiopia. PLoS ONE. 2015;10:e0140780.CrossRefPubMedPubMedCentral
79.
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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
80.
go back to reference Bell AS, de Roode JC, Sim D, Read AF. Within-host competition in genetically diverse malaria infections: parasite virulence and competitive success. Evolution. 2006;60:1358–71.CrossRefPubMed Bell AS, de Roode JC, Sim D, Read AF. Within-host competition in genetically diverse malaria infections: parasite virulence and competitive success. Evolution. 2006;60:1358–71.CrossRefPubMed
81.
go back to reference Bushman M, Morton L, Duah N, Quashie N, Abuaku B, Koram KA, et al. Within-host competition and drug resistance in the human malaria parasite Plasmodium falciparum. Proc Biol Sci. 2016;283:20153038.CrossRefPubMedPubMedCentral Bushman M, Morton L, Duah N, Quashie N, Abuaku B, Koram KA, et al. Within-host competition and drug resistance in the human malaria parasite Plasmodium falciparum. Proc Biol Sci. 2016;283:20153038.CrossRefPubMedPubMedCentral
82.
go back to reference Branch OH, Takala S, Kariuki S, Nahlen BL, Kolczak M, Hawley W, et al. Plasmodium falciparum genotypes, low complexity of infection, and resistance to subsequent malaria in participants in the Asembo Bay Cohort Project. Infect Immun. 2001;69:7783–92.CrossRefPubMedPubMedCentral Branch OH, Takala S, Kariuki S, Nahlen BL, Kolczak M, Hawley W, et al. Plasmodium falciparum genotypes, low complexity of infection, and resistance to subsequent malaria in participants in the Asembo Bay Cohort Project. Infect Immun. 2001;69:7783–92.CrossRefPubMedPubMedCentral
83.
go back to reference Nkhoma SC, Nair S, Cheeseman IH, Rohr-Allegrini C, Singlam S, Nosten F, et al. Close kinship within multiple-genotype malaria parasite infections. Proc Biol Sci. 2012;279:2589–98.CrossRefPubMedPubMedCentral Nkhoma SC, Nair S, Cheeseman IH, Rohr-Allegrini C, Singlam S, Nosten F, et al. Close kinship within multiple-genotype malaria parasite infections. Proc Biol Sci. 2012;279:2589–98.CrossRefPubMedPubMedCentral
84.
go back to reference Oyola SO, Gu Y, Manske M, Otto TD, O’Brien J, Alcock D, et al. Efficient depletion of host DNA contamination in malaria clinical sequencing. J Clin Microbiol. 2013;51:745–51.CrossRefPubMedPubMedCentral Oyola SO, Gu Y, Manske M, Otto TD, O’Brien J, Alcock D, et al. Efficient depletion of host DNA contamination in malaria clinical sequencing. J Clin Microbiol. 2013;51:745–51.CrossRefPubMedPubMedCentral
Metadata
Title
Multiplicity and molecular epidemiology of Plasmodium vivax and Plasmodium falciparum infections in East Africa
Authors
Daibin Zhong
Eugenia Lo
Xiaoming Wang
Delenasaw Yewhalaw
Guofa Zhou
Harrysone E. Atieli
Andrew Githeko
Elizabeth Hemming-Schroeder
Ming-Chieh Lee
Yaw Afrane
Guiyun Yan
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2018
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-018-2337-y

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