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Published in: Malaria Journal 1/2020

01-12-2020 | Plasmodium Falciparum | Research

Molecular epidemiology of Plasmodium falciparum by multiplexed amplicon deep sequencing in Senegal

Published in: Malaria Journal | Issue 1/2020

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Abstract

Background

Molecular epidemiology can provide important information regarding the genetic diversity and transmission of Plasmodium falciparum, which can assist in designing and monitoring elimination efforts. However, malaria molecular epidemiology including understanding the genetic diversity of the parasite and performing molecular surveillance of transmission has been poorly documented in Senegal. Next Generation Sequencing (NGS) offers a practical, fast and high-throughput approach to understand malaria population genetics. This study aims to unravel the population structure of P. falciparum and to estimate the allelic diversity, multiplicity of infection (MOI), and evolutionary patterns of the malaria parasite using the NGS platform.

Methods

Multiplex amplicon deep sequencing of merozoite surface protein 1 (PfMSP1) and merozoite surface protein 2 (PfMSP2) in fifty-three P. falciparum isolates from two epidemiologically different areas in the South and North of Senegal, was carried out.

Results

A total of 76 Pfmsp1 and 116 Pfmsp2 clones were identified and 135 different alleles were found, 56 and 79 belonged to the pfmsp1 and pfmsp2 genes, respectively. K1 and IC3D7 allelic families were most predominant in both sites. The local haplotype diversity (Hd) and nucleotide diversity (π) were higher in the South than in the North for both genes. For pfmsp1, a high positive Tajima’s D (TD) value was observed in the South (D = 2.0453) while negative TD value was recorded in the North (D = − 1.46045) and F-Statistic (Fst) was 0.19505. For pfmsp2, non-directional selection was found with a highly positive TD test in both areas and Fst was 0.02111. The mean MOI for both genes was 3.07 and 1.76 for the South and the North, respectively, with a statistically significant difference between areas (p = 0.001).

Conclusion

This study revealed a high genetic diversity of pfmsp1 and pfmsp2 genes and low genetic differentiation in P. falciparum population in Senegal. The MOI means were significantly different between the Southern and Northern areas. Findings also showed that multiplexed amplicon deep sequencing is a useful technique to investigate genetic diversity and molecular epidemiology of P. falciparum infections.
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Literature
2.
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
3.
go back to reference Khaireh BA, Assefa A, Guessod HH, Basco LK, Khaireh MA, Pascual A, et al. Population genetics analysis during the elimination process of Plasmodium falciparum in Djibouti. Malar J. 2013;12:201. PubMedPubMedCentralCrossRef Khaireh BA, Assefa A, Guessod HH, Basco LK, Khaireh MA, Pascual A, et al. Population genetics analysis during the elimination process of Plasmodium falciparum in Djibouti. Malar J. 2013;12:201. PubMedPubMedCentralCrossRef
4.
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
5.
go back to reference Mohd Abd Razak MR, 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. Mohd Abd Razak MR, 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.
6.
go back to reference Arnott A, Barry AE, Reeder JC. Understanding the population genetics of Plasmodium vivax is essential for malaria control and elimination. Malar J. 2012;11:14. PubMedPubMedCentralCrossRef Arnott A, Barry AE, Reeder JC. Understanding the population genetics of Plasmodium vivax is essential for malaria control and elimination. Malar J. 2012;11:14. PubMedPubMedCentralCrossRef
7.
go back to reference Daniels RF, Schaffner SF, Wenger EA, Proctor JL, Chang H-H, Wong W, et al. Modeling malaria genomics reveals transmission decline and rebound in Senegal. Proc Natl Acad Sci USA. 2015;112:7067–72. PubMedCrossRefPubMedCentral Daniels RF, Schaffner SF, Wenger EA, Proctor JL, Chang H-H, Wong W, et al. Modeling malaria genomics reveals transmission decline and rebound in Senegal. Proc Natl Acad Sci USA. 2015;112:7067–72. PubMedCrossRefPubMedCentral
8.
go back to reference Niang M, Thiam LG, Loucoubar C, Sow A, Sadio BD, Diallo M, et al. Spatio-temporal analysis of the genetic diversity and complexity of Plasmodium falciparum infections in Kédougou Southeastern. Senegal Parasit Vectors. 2017;10:33. PubMedCrossRef Niang M, Thiam LG, Loucoubar C, Sow A, Sadio BD, Diallo M, et al. Spatio-temporal analysis of the genetic diversity and complexity of Plasmodium falciparum infections in Kédougou Southeastern. Senegal Parasit Vectors. 2017;10:33. PubMedCrossRef
9.
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. PubMedCrossRef 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. PubMedCrossRef
10.
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 Biol Chem. 2016;291:7703–15. PubMedPubMedCentralCrossRef 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 Biol Chem. 2016;291:7703–15. PubMedPubMedCentralCrossRef
11.
go back to reference Baldwin MR, Li X, Hanada T, Liu S-C, Chishti AH. Merozoite surface protein 1 recognition of host glycophorin A mediates malaria parasite invasion of red blood cells. Blood. 2015;125:2704–11. PubMedPubMedCentralCrossRef Baldwin MR, Li X, Hanada T, Liu S-C, Chishti AH. Merozoite surface protein 1 recognition of host glycophorin A mediates malaria parasite invasion of red blood cells. Blood. 2015;125:2704–11. PubMedPubMedCentralCrossRef
12.
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. PubMedCrossRef 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. PubMedCrossRef
13.
go back to reference Mwingira F, Nkwengulila G, Schoepflin S, Sumari D, Beck H-P, Snounou G, et al. allele frequency and diversity in sub-Saharan Africa. Malar J. 2011;10:79. PubMedPubMedCentralCrossRef Mwingira F, Nkwengulila G, Schoepflin S, Sumari D, Beck H-P, Snounou G, et al. allele frequency and diversity in sub-Saharan Africa. Malar J. 2011;10:79. PubMedPubMedCentralCrossRef
14.
go back to reference Ahmedou Salem MSO, Ndiaye M, OuldAbdallahi M, Lekweiry KM, Bogreau H, Konaté L, et al. Polymorphism of the merozoite surface protein-1 block 2 region in Plasmodium falciparum isolates from Mauritania. Malar J. 2014;13:26. PubMedPubMedCentralCrossRef Ahmedou Salem MSO, Ndiaye M, OuldAbdallahi M, Lekweiry KM, Bogreau H, Konaté L, et al. Polymorphism of the merozoite surface protein-1 block 2 region in Plasmodium falciparum isolates from Mauritania. Malar J. 2014;13:26. PubMedPubMedCentralCrossRef
15.
go back to reference Soulama I, Nébié I, Ouédraogo A, Gansane A, Diarra A, Tiono AB, et al. Plasmodium falciparum genotypes diversity in symptomatic malaria of children living in an urban and a rural setting in Burkina Faso. Malar J. 2009;8:135. PubMedPubMedCentralCrossRef Soulama I, Nébié I, Ouédraogo A, Gansane A, Diarra A, Tiono AB, et al. Plasmodium falciparum genotypes diversity in symptomatic malaria of children living in an urban and a rural setting in Burkina Faso. Malar J. 2009;8:135. PubMedPubMedCentralCrossRef
16.
go back to reference Yavo W, Konaté A, Mawili-Mboumba DP, Kassi FK, Tshibola Mbuyi ML, Angora EK, et al. Genetic polymorphism of msp1 and msp2 in Plasmodium falciparum isolates from Côte d’Ivoire versus Gabon. J Parasitol Res. 2016;2016:3074803. PubMedPubMedCentralCrossRef Yavo W, Konaté A, Mawili-Mboumba DP, Kassi FK, Tshibola Mbuyi ML, Angora EK, et al. Genetic polymorphism of msp1 and msp2 in Plasmodium falciparum isolates from Côte d’Ivoire versus Gabon. J Parasitol Res. 2016;2016:3074803. PubMedPubMedCentralCrossRef
17.
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. PubMedPubMedCentralCrossRef 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. PubMedPubMedCentralCrossRef
18.
go back to reference Bouyou-Akotet MK, M’Bondoukwé 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. PubMedCrossRef Bouyou-Akotet MK, M’Bondoukwé 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. PubMedCrossRef
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;61:01500–16. CrossRef 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;61:01500–16. CrossRef
20.
go back to reference Greenhouse B, Myrick A, Dokomajilar C, Woo JM, Carlson EJ, Rosenthal PJ, et al. Validation of microsatellite markers for use in genotyping polyclonal Plasmodium falciparum infections. Am J Trop Med Hyg. 2006;75:836–42. PubMedCrossRef Greenhouse B, Myrick A, Dokomajilar C, Woo JM, Carlson EJ, Rosenthal PJ, et al. Validation of microsatellite markers for use in genotyping polyclonal Plasmodium falciparum infections. Am J Trop Med Hyg. 2006;75:836–42. PubMedCrossRef
21.
go back to reference Hosseinzadeh-Colagar A, Haghighatnia MJ, Amiri Z, Mohadjerani M, Tafrihi M. Microsatellite (SSR) amplification by PCR usually led to polymorphic bands: evidence which shows replication slippage occurs in extend or nascent DNA strands. Mol Biol Res Commun. 2016;5:167–74. PubMedPubMedCentral Hosseinzadeh-Colagar A, Haghighatnia MJ, Amiri Z, Mohadjerani M, Tafrihi M. Microsatellite (SSR) amplification by PCR usually led to polymorphic bands: evidence which shows replication slippage occurs in extend or nascent DNA strands. Mol Biol Res Commun. 2016;5:167–74. PubMedPubMedCentral
22.
go back to reference Van Hong N, Delgado-Ratto C, Thanh PV, Van den Eede P, Guetens P, Binh NTH, et al. Population genetics of Plasmodium vivax in four rural communities in Central Vietnam. PLoS Negl Trop Dis. 2016;10:e0004434. PubMedPubMedCentralCrossRef Van Hong N, Delgado-Ratto C, Thanh PV, Van den Eede P, Guetens P, Binh NTH, et al. Population genetics of Plasmodium vivax in four rural communities in Central Vietnam. PLoS Negl Trop Dis. 2016;10:e0004434. PubMedPubMedCentralCrossRef
23.
go back to reference Papa Mze N, Ndiaye YD, Diedhiou CK, Rahamatou S, Dieye B, Daniels RF, et al. RDTs as a source of DNA to study Plasmodium falciparum drug resistance in isolates from Senegal and the Comoros Islands. Malar J. 2015;14:373. PubMedPubMedCentralCrossRef Papa Mze N, Ndiaye YD, Diedhiou CK, Rahamatou S, Dieye B, Daniels RF, et al. RDTs as a source of DNA to study Plasmodium falciparum drug resistance in isolates from Senegal and the Comoros Islands. Malar J. 2015;14:373. PubMedPubMedCentralCrossRef
24.
go back to reference Zhong D, Lo E, Wang X, Yewhalaw D, Zhou G, Atieli HE, et al. Multiplicity and molecular epidemiology of Plasmodium vivax and Plasmodium falciparum infections in East Africa. Malar J. 2018;17:185. PubMedPubMedCentralCrossRef Zhong D, Lo E, Wang X, Yewhalaw D, Zhou G, Atieli HE, et al. Multiplicity and molecular epidemiology of Plasmodium vivax and Plasmodium falciparum infections in East Africa. Malar J. 2018;17:185. PubMedPubMedCentralCrossRef
25.
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. PubMedCrossRefPubMedCentral 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. PubMedCrossRefPubMedCentral
27.
go back to reference Lerch A, Koepfli C, Hofmann NE, 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;18:64. CrossRef Lerch A, Koepfli C, Hofmann NE, 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;18:64. CrossRef
28.
go back to reference Leclerc MC, Durand P, de Meeûs T, Robert V, Renaud F. Genetic diversity and population structure of Plasmodium falciparum isolates from Dakar, Senegal, investigated from microsatellite and antigen determinant loci. Microb Infect. 2002;4:685–92. CrossRef Leclerc MC, Durand P, de Meeûs T, Robert V, Renaud F. Genetic diversity and population structure of Plasmodium falciparum isolates from Dakar, Senegal, investigated from microsatellite and antigen determinant loci. Microb Infect. 2002;4:685–92. CrossRef
29.
go back to reference Ahouidi AD, Bei AK, Neafsey DE, Sarr O, Volkman S, Milner D, et al. Population genetic analysis of large sequence polymorphisms in Plasmodium falciparum blood-stage antigens. Infect Genet Evol. 2010;10:200–6. PubMedCrossRef Ahouidi AD, Bei AK, Neafsey DE, Sarr O, Volkman S, Milner D, et al. Population genetic analysis of large sequence polymorphisms in Plasmodium falciparum blood-stage antigens. Infect Genet Evol. 2010;10:200–6. PubMedCrossRef
30.
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
31.
go back to reference WHO. Communicable diseases cluster: severe falciparum malaria. Trans R Soc Trop Med Hyg. 2000;94:0S1–S9. WHO. Communicable diseases cluster: severe falciparum malaria. Trans R Soc Trop Med Hyg. 2000;94:0S1–S9.
33.
go back to reference Lucchi NW, Karell MA, Journel I, Rogier E, Goldman I, Ljolje D, et al. PET-PCR method for the molecular detection of malaria parasites in a national malaria surveillance study in Haiti, 2011. Malar J. 2014;13:462. PubMedPubMedCentralCrossRef Lucchi NW, Karell MA, Journel I, Rogier E, Goldman I, Ljolje D, et al. PET-PCR method for the molecular detection of malaria parasites in a national malaria surveillance study in Haiti, 2011. Malar J. 2014;13:462. PubMedPubMedCentralCrossRef
34.
go back to reference Lima GFM de C, Lucchi NW, Silva-Flannery L, Macedo-de-Oliveira A, Hristov AD, Inoue J, et al. Still searching for a suitable molecular test to detect hidden Plasmodium infection: a proposal for blood donor screening in Brazil. PLoS One. 2016;11:e0150391. Lima GFM de C, Lucchi NW, Silva-Flannery L, Macedo-de-Oliveira A, Hristov AD, Inoue J, et al. Still searching for a suitable molecular test to detect hidden Plasmodium infection: a proposal for blood donor screening in Brazil. PLoS One. 2016;11:e0150391.
35.
go back to reference Snounou G, Zhu X, Siripoon N, Jarra W, Thaithong S, Brown KN, et al. Biased distribution of msp1 and msp2 allelic variants in Plasmodium falciparum populations in Thailand. Trans R Soc Trop Med Hyg. 1999;93:369–74. PubMedCrossRef Snounou G, Zhu X, Siripoon N, Jarra W, Thaithong S, Brown KN, et al. Biased distribution of msp1 and msp2 allelic variants in Plasmodium falciparum populations in Thailand. Trans R Soc Trop Med Hyg. 1999;93:369–74. PubMedCrossRef
36.
go back to reference Matranga CB, Andersen KG, Winnicki S, Busby M, Gladden AD, Tewhey R, et al. Enhanced methods for unbiased deep sequencing of Lassa and Ebola RNA viruses from clinical and biological samples. Genome Biol. 2014;15:519. PubMedPubMedCentralCrossRef Matranga CB, Andersen KG, Winnicki S, Busby M, Gladden AD, Tewhey R, et al. Enhanced methods for unbiased deep sequencing of Lassa and Ebola RNA viruses from clinical and biological samples. Genome Biol. 2014;15:519. PubMedPubMedCentralCrossRef
38.
go back to reference Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol. 2011;29:644–52. PubMedPubMedCentralCrossRef Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol. 2011;29:644–52. PubMedPubMedCentralCrossRef
39.
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.
40.
go back to reference Librado P, Rozas J. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics. 2009;25:1451–2. PubMedCrossRef Librado P, Rozas J. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics. 2009;25:1451–2. PubMedCrossRef
41.
go back to reference Tajima F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics. 1989;123:585–95. PubMedPubMedCentral Tajima F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics. 1989;123:585–95. PubMedPubMedCentral
42.
go back to reference Weir BS, Cockerham CC. Estimating f-statistics for the analysis of population structure. Evolution. 1984;38:1358–70. PubMed Weir BS, Cockerham CC. Estimating f-statistics for the analysis of population structure. Evolution. 1984;38:1358–70. PubMed
43.
go back to reference Agyeman-Budu A, Brown C, Adjei G, Adams M, Dosoo D, Dery D, et al. Trends in multiplicity of Plasmodium falciparum infections among asymptomatic residents in the middle belt of Ghana. Malar J. 2013;12:22. PubMedPubMedCentralCrossRef Agyeman-Budu A, Brown C, Adjei G, Adams M, Dosoo D, Dery D, et al. Trends in multiplicity of Plasmodium falciparum infections among asymptomatic residents in the middle belt of Ghana. Malar J. 2013;12:22. PubMedPubMedCentralCrossRef
44.
go back to reference Lê HG, Kang JM, Jun H, Lee J, Thái TL, Myint MK, et al. Changing pattern of the genetic diversities of Plasmodium falciparum merozoite surface protein-1 and merozoite surface protein-2 in Myanmar isolates. Malar J. 2019;18:241. PubMedPubMedCentralCrossRef Lê HG, Kang JM, Jun H, Lee J, Thái TL, Myint MK, et al. Changing pattern of the genetic diversities of Plasmodium falciparum merozoite surface protein-1 and merozoite surface protein-2 in Myanmar isolates. Malar J. 2019;18:241. PubMedPubMedCentralCrossRef
45.
go back to reference Aspeling-Jones H, Conway DJ. An expanded global inventory of allelic variation in the most extremely polymorphic region of Plasmodium falciparum merozoite surface protein 1 provided by short read sequence data. Malar J. 2018;17:345. PubMedPubMedCentralCrossRef Aspeling-Jones H, Conway DJ. An expanded global inventory of allelic variation in the most extremely polymorphic region of Plasmodium falciparum merozoite surface protein 1 provided by short read sequence data. Malar J. 2018;17:345. PubMedPubMedCentralCrossRef
46.
go back to reference Ferreira M. Sequence diversity and evolution of the malaria vaccine candidate merozoite surface protein-1 (MSP-1) of Plasmodium falciparum. Gene. 2003;304:65–75. PubMedCrossRef Ferreira M. Sequence diversity and evolution of the malaria vaccine candidate merozoite surface protein-1 (MSP-1) of Plasmodium falciparum. Gene. 2003;304:65–75. PubMedCrossRef
47.
go back to reference Kang JM, Moon SU, Kim JY, Cho SH, Lin K, Sohn WM, et al. Genetic polymorphism of merozoite surface protein-1 and merozoite surface protein-2 in Plasmodium falciparum field isolates from Myanmar. Malar J. 2010;9:131. PubMedPubMedCentralCrossRef Kang JM, Moon SU, Kim JY, Cho SH, Lin K, Sohn WM, et al. Genetic polymorphism of merozoite surface protein-1 and merozoite surface protein-2 in Plasmodium falciparum field isolates from Myanmar. Malar J. 2010;9:131. PubMedPubMedCentralCrossRef
48.
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
49.
go back to reference Ghansah A, Amenga-Etego L, Amambua-Ngwa A, Andagalu B, Apinjoh T, Bouyou-Akotet M, et al. Monitoring parasite diversity for malaria elimination in sub-Saharan Africa. Science. 2014;345:1297–8. PubMedPubMedCentralCrossRef Ghansah A, Amenga-Etego L, Amambua-Ngwa A, Andagalu B, Apinjoh T, Bouyou-Akotet M, et al. Monitoring parasite diversity for malaria elimination in sub-Saharan Africa. Science. 2014;345:1297–8. PubMedPubMedCentralCrossRef
50.
go back to reference Osier FHA, Weedall GD, Verra F, Murungi L, Tetteh KKA, Bull P, et al. Allelic diversity and naturally acquired allele-specific antibody responses to Plasmodium falciparum apical membrane antigen 1 in Kenya. Infect Immun. 2010;78:4625–33. PubMedPubMedCentralCrossRef Osier FHA, Weedall GD, Verra F, Murungi L, Tetteh KKA, Bull P, et al. Allelic diversity and naturally acquired allele-specific antibody responses to Plasmodium falciparum apical membrane antigen 1 in Kenya. Infect Immun. 2010;78:4625–33. PubMedPubMedCentralCrossRef
51.
go back to reference Oyebola KM, Idowu ET, Olukosi YA, Awolola TS, Amambua-Ngwa A. Pooled-DNA sequencing identifies genomic regions of selection in Nigerian isolates of Plasmodium falciparum. Parasit Vectors. 2017;10:320. PubMedPubMedCentralCrossRef Oyebola KM, Idowu ET, Olukosi YA, Awolola TS, Amambua-Ngwa A. Pooled-DNA sequencing identifies genomic regions of selection in Nigerian isolates of Plasmodium falciparum. Parasit Vectors. 2017;10:320. PubMedPubMedCentralCrossRef
52.
go back to reference Molina-Cruz A, Barillas-Mury C. The remarkable journey of adaptation of the Plasmodium falciparum malaria parasite to New World anopheline mosquitoes. Mem Inst Oswaldo Cruz. 2014;109:662–7. PubMedPubMedCentralCrossRef Molina-Cruz A, Barillas-Mury C. The remarkable journey of adaptation of the Plasmodium falciparum malaria parasite to New World anopheline mosquitoes. Mem Inst Oswaldo Cruz. 2014;109:662–7. PubMedPubMedCentralCrossRef
53.
go back to reference Rono MK, Nyonda MA, Simam JJ, Ngoi JM, Mok S, Kortok MM, et al. Adaptation of Plasmodium falciparum to its transmission environment. Nat Ecol Evol. 2018;2:377–87. PubMedCrossRef Rono MK, Nyonda MA, Simam JJ, Ngoi JM, Mok S, Kortok MM, et al. Adaptation of Plasmodium falciparum to its transmission environment. Nat Ecol Evol. 2018;2:377–87. PubMedCrossRef
54.
go back to reference Chenet SM, Schneider KA, Villegas L, Escalante AA. Local population structure of Plasmodium: impact on malaria control and elimination. Malar J. 2012;11:412. PubMedPubMedCentralCrossRef Chenet SM, Schneider KA, Villegas L, Escalante AA. Local population structure of Plasmodium: impact on malaria control and elimination. Malar J. 2012;11:412. PubMedPubMedCentralCrossRef
55.
go back to reference Contamin H, Fandeur T, Rogier C, Bonnefoy S, Konate L, Trape JF, et al. Different genetic characteristics of Plasmodium falciparum isolates collected during successive clinical Malaria episodes in Senegalese children. Am J Trop Med Hyg. 1996;54:632–43. PubMedCrossRef Contamin H, Fandeur T, Rogier C, Bonnefoy S, Konate L, Trape JF, et al. Different genetic characteristics of Plasmodium falciparum isolates collected during successive clinical Malaria episodes in Senegalese children. Am J Trop Med Hyg. 1996;54:632–43. PubMedCrossRef
56.
go back to reference Hastings IM, D’Alessandro U. Modelling a predictable disaster: the rise and spread of drug-resistant malaria. Parasitol Today. 2000;16:340–7. PubMedCrossRef Hastings IM, D’Alessandro U. Modelling a predictable disaster: the rise and spread of drug-resistant malaria. Parasitol Today. 2000;16:340–7. PubMedCrossRef
57.
go back to reference Atroosh WM, Al-Mekhlafi HM, Mahdy MA, Saif-Ali R, Al-Mekhlafi AM, Surin J. Genetic diversity of Plasmodium falciparum isolates from Pahang, Malaysia based on MSP-1 and MSP-2 genes. Parasit Vectors. 2011;4:233. PubMedPubMedCentralCrossRef Atroosh WM, Al-Mekhlafi HM, Mahdy MA, Saif-Ali R, Al-Mekhlafi AM, Surin J. Genetic diversity of Plasmodium falciparum isolates from Pahang, Malaysia based on MSP-1 and MSP-2 genes. Parasit Vectors. 2011;4:233. PubMedPubMedCentralCrossRef
58.
go back to reference Wanji S, Kengne-Ouafo AJ, Eyong EEJ, Kimbi HK, Tendongfor N, Ndamukong-Nyanga JL, et al. Genetic diversity of Plasmodium falciparum merozoite surface protein-1 block 2 in sites of contrasting altitudes and malaria endemicities in the Mount Cameroon region. Am J Trop Med Hyg. 2012;86:64–774. CrossRef Wanji S, Kengne-Ouafo AJ, Eyong EEJ, Kimbi HK, Tendongfor N, Ndamukong-Nyanga JL, et al. Genetic diversity of Plasmodium falciparum merozoite surface protein-1 block 2 in sites of contrasting altitudes and malaria endemicities in the Mount Cameroon region. Am J Trop Med Hyg. 2012;86:64–774. CrossRef
59.
go back to reference Nkhoma SC, Nair S, Al-Saai S, Ashley E, McGready R, Phyo AP, et al. Population genetic correlates of declining transmission in a human pathogen. Mol Ecol. 2013;22:273–85. PubMedCrossRef Nkhoma SC, Nair S, Al-Saai S, Ashley E, McGready R, Phyo AP, et al. Population genetic correlates of declining transmission in a human pathogen. Mol Ecol. 2013;22:273–85. PubMedCrossRef
60.
go back to reference Pumpaibool T, Arnathau C, Durand P, Kanchanakhan N, Siripoon N, Suegorn A, et al. Genetic diversity and population structure of Plasmodium falciparum in Thailand, a low transmission country. Malar J. 2009;8:155. PubMedPubMedCentralCrossRef Pumpaibool T, Arnathau C, Durand P, Kanchanakhan N, Siripoon N, Suegorn A, et al. Genetic diversity and population structure of Plasmodium falciparum in Thailand, a low transmission country. Malar J. 2009;8:155. PubMedPubMedCentralCrossRef
61.
go back to reference Noviyanti R, Coutrier F, Utami RAS, 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. Noviyanti R, Coutrier F, Utami RAS, 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.
62.
go back to reference Lindblade KA, Steinhardt L, Samuels A, Slutsker L, Kachur P. The silent threat: asymptomatic parasitemia and malaria transmission. Expert Rev Anti Infect Ther. 2013;11:623–63. PubMedCrossRef Lindblade KA, Steinhardt L, Samuels A, Slutsker L, Kachur P. The silent threat: asymptomatic parasitemia and malaria transmission. Expert Rev Anti Infect Ther. 2013;11:623–63. PubMedCrossRef
Metadata
Title
Molecular epidemiology of Plasmodium falciparum by multiplexed amplicon deep sequencing in Senegal
Publication date
01-12-2020
Published in
Malaria Journal / Issue 1/2020
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-020-03471-7

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