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Published in: Malaria Journal 1/2019

Open Access 01-12-2019 | Plasmodium Falciparum | Review

Genetic diversity and drug resistance surveillance of Plasmodium falciparum for malaria elimination: is there an ideal tool for resource-limited sub-Saharan Africa?

Authors: Tobias O. Apinjoh, Amed Ouattara, Vincent P. K. Titanji, Abdoulaye Djimde, Alfred Amambua-Ngwa

Published in: Malaria Journal | Issue 1/2019

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Abstract

The intensification of malaria control interventions has resulted in its global decline, but it remains a significant public health burden especially in sub-Saharan Africa (sSA). Knowledge on the parasite diversity, its transmission dynamics, mechanisms of adaptation to environmental and interventional pressures could help refine or develop new control and elimination strategies. Critical to this is the accurate assessment of the parasite’s genetic diversity and monitoring of genetic markers of anti-malarial resistance across all susceptible populations. Such wide molecular surveillance will require selected tools and approaches from a variety of ever evolving advancements in technology and the changing epidemiology of malaria. The choice of an effective approach for specific endemic settings remains challenging, particularly for countries in sSA with limited access to advanced technologies. This article examines the current strategies and tools for Plasmodium falciparum genetic diversity typing and resistance monitoring and proposes how the different tools could be employed in resource-poor settings. Advanced approaches enabling targeted deep sequencing is valued as a sensitive method for assessing drug resistance and parasite diversity but remains out of the reach of most laboratories in sSA due to the high cost of development and maintenance. It is, however, feasible to equip a limited number of laboratories as Centres of Excellence in Africa (CEA), which will receive and process samples from a network of peripheral laboratories in the continent. Cheaper, sensitive and portable real-time PCR methods can be used in peripheral laboratories to pre-screen and select samples for targeted deep sequence or genome wide analyses at these CEAs.
Literature
1.
go back to reference WHO. World malaria report 2018. Geneva: World Health Organization; 2018. WHO. World malaria report 2018. Geneva: World Health Organization; 2018.
2.
go back to reference Bhatt S, Weiss DJ, Cameron E, Bisanzio D, Mappin B, Dalrymple U, et al. The effect of malaria control on Plasmodium falciparum in Africa between 2000 and 2015. Nature. 2015;526:207211.CrossRef Bhatt S, Weiss DJ, Cameron E, Bisanzio D, Mappin B, Dalrymple U, et al. The effect of malaria control on Plasmodium falciparum in Africa between 2000 and 2015. Nature. 2015;526:207211.CrossRef
3.
go back to reference WHO. World malaria report 2016. Geneva: World Health Organization; 2016. WHO. World malaria report 2016. Geneva: World Health Organization; 2016.
4.
go back to reference Apinjoh TO, Anchang-Kimbi JK, Mugri RN, Tangoh DA, Nyingchu RV, Chi HF, et al. The effect of insecticide treated nets (ITNs) on Plasmodium falciparum infection in rural and semi-urban communities in the south west region of Cameroon. PLoS ONE. 2015;10:e0116300.PubMedPubMedCentralCrossRef Apinjoh TO, Anchang-Kimbi JK, Mugri RN, Tangoh DA, Nyingchu RV, Chi HF, et al. The effect of insecticide treated nets (ITNs) on Plasmodium falciparum infection in rural and semi-urban communities in the south west region of Cameroon. PLoS ONE. 2015;10:e0116300.PubMedPubMedCentralCrossRef
5.
go back to reference Griffin JT, Ferguson NM, Ghani AC. Estimates of the changing age-burden of Plasmodium falciparum malaria disease in sub-Saharan Africa. Nat Commun. 2014;5:3136.PubMedCrossRef Griffin JT, Ferguson NM, Ghani AC. Estimates of the changing age-burden of Plasmodium falciparum malaria disease in sub-Saharan Africa. Nat Commun. 2014;5:3136.PubMedCrossRef
6.
go back to reference Trape JF, Tall A, Diagne N, Ndiath O, Ly AB, Faye J, et al. Malaria morbidity and pyrethroid resistance after the introduction of insecticide-treated bednets and artemisinin-based combination therapies: a longitudinal study. Lancet Infect Dis. 2011;11:925–32.PubMedCrossRef Trape JF, Tall A, Diagne N, Ndiath O, Ly AB, Faye J, et al. Malaria morbidity and pyrethroid resistance after the introduction of insecticide-treated bednets and artemisinin-based combination therapies: a longitudinal study. Lancet Infect Dis. 2011;11:925–32.PubMedCrossRef
7.
go back to reference Cohen JM, Smith DL, Cotter C, Ward A, Yamey G, Sabot OJ, et al. Malaria resurgence: a systematic review and assessment of its causes. Malar J. 2012;11:122.PubMedPubMedCentralCrossRef Cohen JM, Smith DL, Cotter C, Ward A, Yamey G, Sabot OJ, et al. Malaria resurgence: a systematic review and assessment of its causes. Malar J. 2012;11:122.PubMedPubMedCentralCrossRef
8.
go back to reference Neafsey DE, Schaffner SF, Volkman SK, Park D, Montgomery P, Milner DA Jr, et al. Genome-wide SNP genotyping highlights the role of natural selection in Plasmodium falciparum population divergence. Genome Biol. 2008;9:R171.PubMedPubMedCentralCrossRef Neafsey DE, Schaffner SF, Volkman SK, Park D, Montgomery P, Milner DA Jr, et al. Genome-wide SNP genotyping highlights the role of natural selection in Plasmodium falciparum population divergence. Genome Biol. 2008;9:R171.PubMedPubMedCentralCrossRef
9.
go back to reference Volkman SK, Sabeti PC, DeCaprio D, Neafsey DE, Schaffner SF, Milner DA Jr, et al. A genome-wide map of diversity in Plasmodium falciparum. Nat Genet. 2007;39:113–9.PubMedCrossRef Volkman SK, Sabeti PC, DeCaprio D, Neafsey DE, Schaffner SF, Milner DA Jr, et al. A genome-wide map of diversity in Plasmodium falciparum. Nat Genet. 2007;39:113–9.PubMedCrossRef
10.
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;487:375–9.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;487:375–9.PubMedPubMedCentralCrossRef
12.
go back to reference Takala SL, Plowe CV. Genetic diversity and malaria vaccine design, testing and efficacy: preventing and overcoming ‘vaccine resistant malaria’. Parasite Immunol. 2009;31:560–73.PubMedPubMedCentralCrossRef Takala SL, Plowe CV. Genetic diversity and malaria vaccine design, testing and efficacy: preventing and overcoming ‘vaccine resistant malaria’. Parasite Immunol. 2009;31:560–73.PubMedPubMedCentralCrossRef
13.
go back to reference Watson OJ, Slater HC, Verity R, Parr JB, Mwandagalirwa MK, Tshefu A, et al. Modelling the drivers of the spread of Plasmodium falciparum hrp2 gene deletions in sub-Saharan Africa. Elife. 2017;6:e25008.PubMedPubMedCentralCrossRef Watson OJ, Slater HC, Verity R, Parr JB, Mwandagalirwa MK, Tshefu A, et al. Modelling the drivers of the spread of Plasmodium falciparum hrp2 gene deletions in sub-Saharan Africa. Elife. 2017;6:e25008.PubMedPubMedCentralCrossRef
14.
go back to reference Molina-Cruz A, Canepa GE, Kamath N, Pavlovic NV, Mu J, Ramphul UN, et al. Plasmodium evasion of mosquito immunity and global malaria transmission: the lock-and-key theory. Proc Natl Acad Sci USA. 2015;112:15178–83.PubMedCrossRefPubMedCentral Molina-Cruz A, Canepa GE, Kamath N, Pavlovic NV, Mu J, Ramphul UN, et al. Plasmodium evasion of mosquito immunity and global malaria transmission: the lock-and-key theory. Proc Natl Acad Sci USA. 2015;112:15178–83.PubMedCrossRefPubMedCentral
15.
16.
go back to reference WHO. Seasonal malaria chemoprevention (SMC) for Plasmodium falciparum malaria control in highly seasonal transmission areas of the Sahel sub-region in Africa. Geneva: World Health Organization; 2012. WHO. Seasonal malaria chemoprevention (SMC) for Plasmodium falciparum malaria control in highly seasonal transmission areas of the Sahel sub-region in Africa. Geneva: World Health Organization; 2012.
17.
go back to reference WHO, Global Malaria Programme. The role of mass drug administration, mass screening and treatment, and focal screening and treatment for malaria: recommendations. Geneva: World Health Organization; 2015. WHO, Global Malaria Programme. The role of mass drug administration, mass screening and treatment, and focal screening and treatment for malaria: recommendations. Geneva: World Health Organization; 2015.
18.
go back to reference WHO. Guidelines for the treatment of malaria. 3rd ed. Geneva: World Health Organization; 2015. WHO. Guidelines for the treatment of malaria. 3rd ed. Geneva: World Health Organization; 2015.
19.
go back to reference WHO. Global report on antimalarial efficacy and drug resistance: 2000–2010. Geneva: World Health Organization; 2010. WHO. Global report on antimalarial efficacy and drug resistance: 2000–2010. Geneva: World Health Organization; 2010.
20.
go back to reference Nosten F, White NJ. Artemisinin-based combination treatment of falciparum malaria. Am J Trop Med Hyg. 2007;77:181–92.PubMedCrossRef Nosten F, White NJ. Artemisinin-based combination treatment of falciparum malaria. Am J Trop Med Hyg. 2007;77:181–92.PubMedCrossRef
21.
go back to reference Dondorp AM, Nosten F, Yi P, Das D, Phyo AP, Tarning J, et al. Artemisinin resistance in Plasmodium falciparum malaria. N Engl J Med. 2009;361:455–67.PubMedPubMedCentralCrossRef Dondorp AM, Nosten F, Yi P, Das D, Phyo AP, Tarning J, et al. Artemisinin resistance in Plasmodium falciparum malaria. N Engl J Med. 2009;361:455–67.PubMedPubMedCentralCrossRef
23.
go back to reference Na-Bangchang K, Muhamad P, Ruaengweerayut R, Chaijaroenkul W, Karbwang J. Identification of resistance of Plasmodium falciparum to artesunate–mefloquine combination in an area along the Thai-Myanmar border: integration of clinico-parasitological response, systemic drug exposure, and in vitro parasite sensitivity. Malar J. 2013;12:263.PubMedPubMedCentralCrossRef Na-Bangchang K, Muhamad P, Ruaengweerayut R, Chaijaroenkul W, Karbwang J. Identification of resistance of Plasmodium falciparum to artesunate–mefloquine combination in an area along the Thai-Myanmar border: integration of clinico-parasitological response, systemic drug exposure, and in vitro parasite sensitivity. Malar J. 2013;12:263.PubMedPubMedCentralCrossRef
24.
go back to reference Amaratunga C, Lim P, Suon S, Sreng S, Mao S, Sopha C, et al. Dihydroartemisinin–piperaquine resistance in Plasmodium falciparum malaria in Cambodia: a multisite prospective cohort study. Lancet Infect Dis. 2016;16:357–65.PubMedPubMedCentralCrossRef Amaratunga C, Lim P, Suon S, Sreng S, Mao S, Sopha C, et al. Dihydroartemisinin–piperaquine resistance in Plasmodium falciparum malaria in Cambodia: a multisite prospective cohort study. Lancet Infect Dis. 2016;16:357–65.PubMedPubMedCentralCrossRef
25.
go back to reference Amato R, Lim P, Miotto O, Amaratunga C, Dek D, Pearson RD, et al. Genetic markers associated with dihydroartemisinin–piperaquine failure in Plasmodium falciparum malaria in Cambodia: a genotype-phenotype association study. Lancet Infect Dis. 2017;17:164–73.PubMedCrossRef Amato R, Lim P, Miotto O, Amaratunga C, Dek D, Pearson RD, et al. Genetic markers associated with dihydroartemisinin–piperaquine failure in Plasmodium falciparum malaria in Cambodia: a genotype-phenotype association study. Lancet Infect Dis. 2017;17:164–73.PubMedCrossRef
26.
go back to reference Omedo I, Mogeni P, Rockett K, Kamau A, Hubbart C, Jeffreys A, et al. Geographic-genetic analysis of Plasmodium falciparum parasite populations from surveys of primary school children in Western Kenya. Wellcome Open Res. 2017;2:29.PubMedPubMedCentralCrossRef Omedo I, Mogeni P, Rockett K, Kamau A, Hubbart C, Jeffreys A, et al. Geographic-genetic analysis of Plasmodium falciparum parasite populations from surveys of primary school children in Western Kenya. Wellcome Open Res. 2017;2:29.PubMedPubMedCentralCrossRef
27.
go back to reference Dwivedi A, Khim N, Reynes C, Ravel P, Ma L, Tichit M, et al. Plasmodium falciparum parasite population structure and gene flow associated to anti-malarial drugs resistance in Cambodia. Malar J. 2016;15:319.PubMedPubMedCentralCrossRef Dwivedi A, Khim N, Reynes C, Ravel P, Ma L, Tichit M, et al. Plasmodium falciparum parasite population structure and gene flow associated to anti-malarial drugs resistance in Cambodia. Malar J. 2016;15:319.PubMedPubMedCentralCrossRef
28.
go back to reference Babiker HA, Walliker D. Current views on the population structure of Plasmodium falciparum: implications for control. Parasitol Today. 1997;13:262–7.PubMedCrossRef Babiker HA, Walliker D. Current views on the population structure of Plasmodium falciparum: implications for control. Parasitol Today. 1997;13:262–7.PubMedCrossRef
29.
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
30.
go back to reference Amambua-Ngwa A, Tetteh KK, Manske M, Gomez-Escobar N, Stewart LB, Deerhake ME, et al. Population genomic scan for candidate signatures of balancing selection to guide antigen characterization in malaria parasites. PLoS Genet. 2012;8:e1002992.PubMedPubMedCentralCrossRef Amambua-Ngwa A, Tetteh KK, Manske M, Gomez-Escobar N, Stewart LB, Deerhake ME, et al. Population genomic scan for candidate signatures of balancing selection to guide antigen characterization in malaria parasites. PLoS Genet. 2012;8:e1002992.PubMedPubMedCentralCrossRef
31.
go back to reference Amambua-Ngwa A, Park DJ, Volkman SK, Barnes KG, Bei AK, Lukens AK, et al. SNP genotyping identifies new signatures of selection in a deep sample of West African Plasmodium falciparum malaria parasites. Mol Biol Evol. 2012;29:3249–53.PubMedPubMedCentralCrossRef Amambua-Ngwa A, Park DJ, Volkman SK, Barnes KG, Bei AK, Lukens AK, et al. SNP genotyping identifies new signatures of selection in a deep sample of West African Plasmodium falciparum malaria parasites. Mol Biol Evol. 2012;29:3249–53.PubMedPubMedCentralCrossRef
32.
go back to reference Van Tyne D, Park DJ, Schaffner SF, Neafsey DE, Angelino E, Cortese JF, et al. Identification and functional validation of the novel antimalarial resistance locus PF10_0355 in Plasmodium falciparum. PLoS Genet. 2011;7:e1001383.PubMedPubMedCentralCrossRef Van Tyne D, Park DJ, Schaffner SF, Neafsey DE, Angelino E, Cortese JF, et al. Identification and functional validation of the novel antimalarial resistance locus PF10_0355 in Plasmodium falciparum. PLoS Genet. 2011;7:e1001383.PubMedPubMedCentralCrossRef
33.
go back to reference Park DJ, Lukens AK, Neafsey DE, Schaffner SF, Chang HH, Valim C, et al. Sequence-based association and selection scans identify drug resistance loci in the Plasmodium falciparum malaria parasite. Proc Natl Acad Sci USA. 2012;109:13052–7.PubMedCrossRefPubMedCentral Park DJ, Lukens AK, Neafsey DE, Schaffner SF, Chang HH, Valim C, et al. Sequence-based association and selection scans identify drug resistance loci in the Plasmodium falciparum malaria parasite. Proc Natl Acad Sci USA. 2012;109:13052–7.PubMedCrossRefPubMedCentral
34.
go back to reference Ariey F, Witkowski B, Amaratunga C, Beghain J, Langlois AC, Khim N, et al. A molecular marker of artemisinin-resistant Plasmodium falciparum malaria. Nature. 2014;505:50–5.PubMedCrossRef Ariey F, Witkowski B, Amaratunga C, Beghain J, Langlois AC, Khim N, et al. A molecular marker of artemisinin-resistant Plasmodium falciparum malaria. Nature. 2014;505:50–5.PubMedCrossRef
35.
go back to reference Ashley EA, Dhorda M, Fairhurst RM, Amaratunga C, Lim P, Suon S, et al. Spread of artemisinin resistance in Plasmodium falciparum malaria. N Engl J Med. 2014;371:411–23.PubMedPubMedCentralCrossRef Ashley EA, Dhorda M, Fairhurst RM, Amaratunga C, Lim P, Suon S, et al. Spread of artemisinin resistance in Plasmodium falciparum malaria. N Engl J Med. 2014;371:411–23.PubMedPubMedCentralCrossRef
36.
go back to reference Imwong M, Suwannasin K, Kunasol C, Sutawong K, Mayxay M, Rekol H, et al. The spread of artemisinin-resistant Plasmodium falciparum in the Greater Mekong subregion: a molecular epidemiology observational study. Lancet Infect Dis. 2017;17:491–7.PubMedPubMedCentralCrossRef Imwong M, Suwannasin K, Kunasol C, Sutawong K, Mayxay M, Rekol H, et al. The spread of artemisinin-resistant Plasmodium falciparum in the Greater Mekong subregion: a molecular epidemiology observational study. Lancet Infect Dis. 2017;17:491–7.PubMedPubMedCentralCrossRef
37.
go back to reference Takala-Harrison S, Jacob CG, Arze C, Cummings MP, Silva JC, Dondorp AM, et al. Independent emergence of artemisinin resistance mutations among Plasmodium falciparum in Southeast Asia. J Infect Dis. 2015;211:670–9.PubMedCrossRef Takala-Harrison S, Jacob CG, Arze C, Cummings MP, Silva JC, Dondorp AM, et al. Independent emergence of artemisinin resistance mutations among Plasmodium falciparum in Southeast Asia. J Infect Dis. 2015;211:670–9.PubMedCrossRef
38.
go back to reference Kamau E, Campino S, Amenga-Etego L, Drury E, Ishengoma D, Johnson K, et al. K13-propeller polymorphisms in Plasmodium falciparum parasites from sub-Saharan Africa. J Infect Dis. 2015;211:1352–5.PubMed Kamau E, Campino S, Amenga-Etego L, Drury E, Ishengoma D, Johnson K, et al. K13-propeller polymorphisms in Plasmodium falciparum parasites from sub-Saharan Africa. J Infect Dis. 2015;211:1352–5.PubMed
39.
go back to reference Wootton JC, Feng X, Ferdig MT, Cooper RA, Mu J, Baruch DI, et al. Genetic diversity and chloroquine selective sweeps in Plasmodium falciparum. Nature. 2002;418:320–3.PubMedCrossRef Wootton JC, Feng X, Ferdig MT, Cooper RA, Mu J, Baruch DI, et al. Genetic diversity and chloroquine selective sweeps in Plasmodium falciparum. Nature. 2002;418:320–3.PubMedCrossRef
40.
go back to reference Roper C, Pearce R, Nair S, Sharp B, Nosten F, Anderson T. Intercontinental spread of pyrimethamine-resistant malaria. Science. 2004;305:1124.PubMedCrossRef Roper C, Pearce R, Nair S, Sharp B, Nosten F, Anderson T. Intercontinental spread of pyrimethamine-resistant malaria. Science. 2004;305:1124.PubMedCrossRef
41.
go back to reference Donnelly MJ, Isaacs AT, Weetman D. Identification, validation, and application of molecular diagnostics for insecticide resistance in malaria vectors. Trends Parasitol. 2016;32:197–206.PubMedCrossRef Donnelly MJ, Isaacs AT, Weetman D. Identification, validation, and application of molecular diagnostics for insecticide resistance in malaria vectors. Trends Parasitol. 2016;32:197–206.PubMedCrossRef
42.
go back to reference Baker J, Ho MF, Pelecanos A, Gatton M, Chen N, Abdullah S, et al. Global sequence variation in the histidine-rich proteins 2 and 3 of Plasmodium falciparum: implications for the performance of malaria rapid diagnostic tests. Malar J. 2010;9:129.PubMedPubMedCentralCrossRef Baker J, Ho MF, Pelecanos A, Gatton M, Chen N, Abdullah S, et al. Global sequence variation in the histidine-rich proteins 2 and 3 of Plasmodium falciparum: implications for the performance of malaria rapid diagnostic tests. Malar J. 2010;9:129.PubMedPubMedCentralCrossRef
43.
go back to reference WHO. Malaria surveillance, monitoring & evaluation: a reference manual. Geneva: World Health Organization; 2018. WHO. Malaria surveillance, monitoring & evaluation: a reference manual. Geneva: World Health Organization; 2018.
44.
go back to reference Nsanzabana C, Djalle D, Guerin PJ, Menard D, Gonzalez IJ. Tools for surveillance of anti-malarial drug resistance: an assessment of the current landscape. Malar J. 2018;17:75.PubMedPubMedCentralCrossRef Nsanzabana C, Djalle D, Guerin PJ, Menard D, Gonzalez IJ. Tools for surveillance of anti-malarial drug resistance: an assessment of the current landscape. Malar J. 2018;17:75.PubMedPubMedCentralCrossRef
45.
go back to reference Witkowski B, Amaratunga C, Khim N, Sreng S, Chim P, Kim S, et al. Novel phenotypic assays for the detection of artemisinin-resistant Plasmodium falciparum malaria in Cambodia: in vitro and ex vivo drug-response studies. Lancet Infect Dis. 2013;13:1043–9.PubMedPubMedCentralCrossRef Witkowski B, Amaratunga C, Khim N, Sreng S, Chim P, Kim S, et al. Novel phenotypic assays for the detection of artemisinin-resistant Plasmodium falciparum malaria in Cambodia: in vitro and ex vivo drug-response studies. Lancet Infect Dis. 2013;13:1043–9.PubMedPubMedCentralCrossRef
46.
go back to reference Plowe CV. Antimalarial drug resistance in Africa: strategies for monitoring and deterrence. Curr Top Microbiol Immunol. 2005;295:55–79.PubMed Plowe CV. Antimalarial drug resistance in Africa: strategies for monitoring and deterrence. Curr Top Microbiol Immunol. 2005;295:55–79.PubMed
47.
go back to reference Plowe CV. Monitoring antimalarial drug resistance: making the most of the tools at hand. J Exp Biol. 2003;206:3745–52.PubMedCrossRef Plowe CV. Monitoring antimalarial drug resistance: making the most of the tools at hand. J Exp Biol. 2003;206:3745–52.PubMedCrossRef
48.
go back to reference WHO. Tools for monitoring antimalarial drug efficacy. Geneva: World Health Organization; 2019. WHO. Tools for monitoring antimalarial drug efficacy. Geneva: World Health Organization; 2019.
49.
go back to reference Kite WA, Melendez-Muniz VA, Moraes Barros RR, Wellems TE, Sa JM. Alternative methods for the Plasmodium falciparum artemisinin ring-stage survival assay with increased simplicity and parasite stage-specificity. Malar J. 2016;15:94.PubMedPubMedCentralCrossRef Kite WA, Melendez-Muniz VA, Moraes Barros RR, Wellems TE, Sa JM. Alternative methods for the Plasmodium falciparum artemisinin ring-stage survival assay with increased simplicity and parasite stage-specificity. Malar J. 2016;15:94.PubMedPubMedCentralCrossRef
50.
go back to reference Duru V, Khim N, Leang R, Kim S, Domergue A, Kloeung N, et al. Plasmodium falciparum dihydroartemisinin–piperaquine failures in Cambodia are associated with mutant K13 parasites presenting high survival rates in novel piperaquine in vitro assays: retrospective and prospective investigations. BMC Med. 2015;13:305.PubMedPubMedCentralCrossRef Duru V, Khim N, Leang R, Kim S, Domergue A, Kloeung N, et al. Plasmodium falciparum dihydroartemisinin–piperaquine failures in Cambodia are associated with mutant K13 parasites presenting high survival rates in novel piperaquine in vitro assays: retrospective and prospective investigations. BMC Med. 2015;13:305.PubMedPubMedCentralCrossRef
51.
go back to reference Woodrow CJ, Dahlstrom S, Cooksey R, Flegg JA, Le Nagard H, Mentre F, et al. High-throughput analysis of antimalarial susceptibility data by the WorldWide Antimalarial Resistance Network (WWARN) in vitro analysis and reporting tool. Antimicrob Agents Chemother. 2013;57:3121–30.PubMedPubMedCentralCrossRef Woodrow CJ, Dahlstrom S, Cooksey R, Flegg JA, Le Nagard H, Mentre F, et al. High-throughput analysis of antimalarial susceptibility data by the WorldWide Antimalarial Resistance Network (WWARN) in vitro analysis and reporting tool. Antimicrob Agents Chemother. 2013;57:3121–30.PubMedPubMedCentralCrossRef
52.
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.PubMedPubMedCentralCrossRef 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.PubMedPubMedCentralCrossRef
53.
go back to reference Marfurt J, Muller I, Sie A, Oa O, Reeder JC, Smith TA, et al. The usefulness of twenty-four molecular markers in predicting treatment outcome with combination therapy of amodiaquine plus sulfadoxine–pyrimethamine against falciparum malaria in Papua New Guinea. Malar J. 2008;7:61.PubMedPubMedCentralCrossRef Marfurt J, Muller I, Sie A, Oa O, Reeder JC, Smith TA, et al. The usefulness of twenty-four molecular markers in predicting treatment outcome with combination therapy of amodiaquine plus sulfadoxine–pyrimethamine against falciparum malaria in Papua New Guinea. Malar J. 2008;7:61.PubMedPubMedCentralCrossRef
54.
go back to reference Miotto O, Amato R, Ashley EA, MacInnis B, Almagro-Garcia J, Amaratunga C, et al. Genetic architecture of artemisinin-resistant Plasmodium falciparum. Nat Genet. 2015;47:226–34.PubMedPubMedCentralCrossRef Miotto O, Amato R, Ashley EA, MacInnis B, Almagro-Garcia J, Amaratunga C, et al. Genetic architecture of artemisinin-resistant Plasmodium falciparum. Nat Genet. 2015;47:226–34.PubMedPubMedCentralCrossRef
55.
go back to reference Veiga MI, Dhingra SK, Henrich PP, Straimer J, Gnadig N, Uhlemann AC, et al. Globally prevalent PfMDR1 mutations modulate Plasmodium falciparum susceptibility to artemisinin-based combination therapies. Nat Commun. 2016;7:11553.PubMedPubMedCentralCrossRef Veiga MI, Dhingra SK, Henrich PP, Straimer J, Gnadig N, Uhlemann AC, et al. Globally prevalent PfMDR1 mutations modulate Plasmodium falciparum susceptibility to artemisinin-based combination therapies. Nat Commun. 2016;7:11553.PubMedPubMedCentralCrossRef
56.
go back to reference Taylor SM, Parobek CM, Aragam N, Ngasala BE, Martensson A, Meshnick SR, et al. Pooled deep sequencing of Plasmodium falciparum isolates: an efficient and scalable tool to quantify prevailing malaria drug-resistance genotypes. J Infect Dis. 2013;208:1998–2006.PubMedPubMedCentralCrossRef Taylor SM, Parobek CM, Aragam N, Ngasala BE, Martensson A, Meshnick SR, et al. Pooled deep sequencing of Plasmodium falciparum isolates: an efficient and scalable tool to quantify prevailing malaria drug-resistance genotypes. J Infect Dis. 2013;208:1998–2006.PubMedPubMedCentralCrossRef
57.
go back to reference Goodwin S, McPherson JD, McCombie WR. Coming of age: ten years of next-generation sequencing technologies. Nat Rev Genet. 2016;17:333–51.PubMedCrossRef Goodwin S, McPherson JD, McCombie WR. Coming of age: ten years of next-generation sequencing technologies. Nat Rev Genet. 2016;17:333–51.PubMedCrossRef
58.
go back to reference Runtuwene LR, Tuda JSB, Mongan AE, Makalowski W, Frith MC, Imwong M, et al. Nanopore sequencing of drug-resistance-associated genes in malaria parasites, Plasmodium falciparum. Sci Rep. 2018;8:8286.PubMedPubMedCentralCrossRef Runtuwene LR, Tuda JSB, Mongan AE, Makalowski W, Frith MC, Imwong M, et al. Nanopore sequencing of drug-resistance-associated genes in malaria parasites, Plasmodium falciparum. Sci Rep. 2018;8:8286.PubMedPubMedCentralCrossRef
59.
go back to reference Quick J, Loman NJ, Duraffour S, Simpson JT, Severi E, Cowley L, et al. Real-time, portable genome sequencing for Ebola surveillance. Nature. 2016;530:228–32.PubMedPubMedCentralCrossRef Quick J, Loman NJ, Duraffour S, Simpson JT, Severi E, Cowley L, et al. Real-time, portable genome sequencing for Ebola surveillance. Nature. 2016;530:228–32.PubMedPubMedCentralCrossRef
60.
go back to reference Achieng AO, Muiruri P, Ingasia LA, Opot BH, Juma DW, Yeda R, et al. Temporal trends in prevalence of Plasmodium falciparum molecular markers selected for by artemether–lumefantrine treatment in pre-ACT and post-ACT parasites in western Kenya. Int J Parasitol Drugs Drug Resist. 2015;5:92–9.PubMedPubMedCentralCrossRef Achieng AO, Muiruri P, Ingasia LA, Opot BH, Juma DW, Yeda R, et al. Temporal trends in prevalence of Plasmodium falciparum molecular markers selected for by artemether–lumefantrine treatment in pre-ACT and post-ACT parasites in western Kenya. Int J Parasitol Drugs Drug Resist. 2015;5:92–9.PubMedPubMedCentralCrossRef
61.
go back to reference Henriques G, Hallett RL, Beshir KB, Gadalla NB, Johnson RE, Burrow R, et al. Directional selection at the pfmdr1, pfcrt, pfubp1, and pfap2mu loci of Plasmodium falciparum in Kenyan children treated with ACT. J Infect Dis. 2014;210:2001–8.PubMedPubMedCentralCrossRef Henriques G, Hallett RL, Beshir KB, Gadalla NB, Johnson RE, Burrow R, et al. Directional selection at the pfmdr1, pfcrt, pfubp1, and pfap2mu loci of Plasmodium falciparum in Kenyan children treated with ACT. J Infect Dis. 2014;210:2001–8.PubMedPubMedCentralCrossRef
62.
go back to reference Okell LC, Reiter LM, Ebbe LS, Baraka V, Bisanzio D, Watson OJ, et al. Emerging implications of policies on malaria treatment: genetic changes in the Pfmdr-1 gene affecting susceptibility to artemether–lumefantrine and artesunate–amodiaquine in Africa. BMJ Glob Health. 2018;3:e000999.PubMedPubMedCentralCrossRef Okell LC, Reiter LM, Ebbe LS, Baraka V, Bisanzio D, Watson OJ, et al. Emerging implications of policies on malaria treatment: genetic changes in the Pfmdr-1 gene affecting susceptibility to artemether–lumefantrine and artesunate–amodiaquine in Africa. BMJ Glob Health. 2018;3:e000999.PubMedPubMedCentralCrossRef
63.
go back to reference Nsanzabana C. Resistance to artemisinin combination therapies (ACTs): do not forget the partner drug! Trop Med Infect Dis. 2019;4:e26.PubMedCrossRef Nsanzabana C. Resistance to artemisinin combination therapies (ACTs): do not forget the partner drug! Trop Med Infect Dis. 2019;4:e26.PubMedCrossRef
64.
go back to reference Ross LS, Dhingra SK, Mok S, Yeo T, Wicht KJ, Kumpornsin K, et al. Emerging Southeast Asian PfCRT mutations confer Plasmodium falciparum resistance to the first-line antimalarial piperaquine. Nat Commun. 2018;9:3314.PubMedPubMedCentralCrossRef Ross LS, Dhingra SK, Mok S, Yeo T, Wicht KJ, Kumpornsin K, et al. Emerging Southeast Asian PfCRT mutations confer Plasmodium falciparum resistance to the first-line antimalarial piperaquine. Nat Commun. 2018;9:3314.PubMedPubMedCentralCrossRef
65.
go back to reference Witkowski B, Duru V, Khim N, Ross LS, Saintpierre B, Beghain J, et al. A surrogate marker of piperaquine-resistant Plasmodium falciparum malaria: a phenotype-genotype association study. Lancet Infect Dis. 2017;17:174–83.PubMedPubMedCentralCrossRef Witkowski B, Duru V, Khim N, Ross LS, Saintpierre B, Beghain J, et al. A surrogate marker of piperaquine-resistant Plasmodium falciparum malaria: a phenotype-genotype association study. Lancet Infect Dis. 2017;17:174–83.PubMedPubMedCentralCrossRef
66.
go back to reference Inoue J, Silva M, Fofana B, Sanogo K, Martensson A, Sagara I, et al. Plasmodium falciparum plasmepsin 2 duplications, West Africa. Emerg Infect Dis. 2018;24:8.CrossRef Inoue J, Silva M, Fofana B, Sanogo K, Martensson A, Sagara I, et al. Plasmodium falciparum plasmepsin 2 duplications, West Africa. Emerg Infect Dis. 2018;24:8.CrossRef
67.
go back to reference WHO. Intermittent preventive treatment in pregnancy (IPTp). Geneva: World Health Organization; 2018. WHO. Intermittent preventive treatment in pregnancy (IPTp). Geneva: World Health Organization; 2018.
68.
go back to reference Gabryszewski SJ, Modchang C, Musset L, Chookajorn T, Fidock DA. Combinatorial genetic modeling of pfcrt-mediated drug resistance evolution in Plasmodium falciparum. Mol Biol Evol. 2016;33:1554–70.PubMedPubMedCentralCrossRef Gabryszewski SJ, Modchang C, Musset L, Chookajorn T, Fidock DA. Combinatorial genetic modeling of pfcrt-mediated drug resistance evolution in Plasmodium falciparum. Mol Biol Evol. 2016;33:1554–70.PubMedPubMedCentralCrossRef
69.
go back to reference Okell LC, Griffin JT, Roper C. Mapping sulphadoxine-pyrimethamine-resistant Plasmodium falciparum malaria in infected humans and in parasite populations in Africa. Sci Rep. 2017;7:7389.PubMedPubMedCentralCrossRef Okell LC, Griffin JT, Roper C. Mapping sulphadoxine-pyrimethamine-resistant Plasmodium falciparum malaria in infected humans and in parasite populations in Africa. Sci Rep. 2017;7:7389.PubMedPubMedCentralCrossRef
70.
go back to reference Viriyakosol S, Siripoon N, Petcharapirat C, Petcharapirat P, Jarra W, Thaithong S, et al. Genotyping of Plasmodium falciparum isolates by the polymerase chain reaction and potential uses in epidemiological studies. Bull World Health Organ. 1995;73:85–95.PubMedPubMedCentral Viriyakosol S, Siripoon N, Petcharapirat C, Petcharapirat P, Jarra W, Thaithong S, et al. Genotyping of Plasmodium falciparum isolates by the polymerase chain reaction and potential uses in epidemiological studies. Bull World Health Organ. 1995;73:85–95.PubMedPubMedCentral
71.
go back to reference Liljander A, Wiklund L, Falk N, Kweku M, Martensson A, Felger I, et al. Optimization and validation of multi-coloured capillary electrophoresis for genotyping of Plasmodium falciparum merozoite surface proteins (msp1 and 2). Malar J. 2009;8:78.PubMedPubMedCentralCrossRef Liljander A, Wiklund L, Falk N, Kweku M, Martensson A, Felger I, et al. Optimization and validation of multi-coloured capillary electrophoresis for genotyping of Plasmodium falciparum merozoite surface proteins (msp1 and 2). Malar J. 2009;8:78.PubMedPubMedCentralCrossRef
72.
go back to reference Juliano JJ, Taylor SM, Meshnick SR. Polymerase chain reaction adjustment in antimalarial trials: molecular malarkey? J Infect Dis. 2009;200:5–7.PubMedCrossRef Juliano JJ, Taylor SM, Meshnick SR. Polymerase chain reaction adjustment in antimalarial trials: molecular malarkey? J Infect Dis. 2009;200:5–7.PubMedCrossRef
73.
go back to reference Beshir KB, Diallo N, Sutherland CJ. Identifying recrudescent Plasmodium falciparum in treated malaria patients by real-time PCR and high resolution melt analysis of genetic diversity. Sci Rep. 2018;8:10097.PubMedPubMedCentralCrossRef Beshir KB, Diallo N, Sutherland CJ. Identifying recrudescent Plasmodium falciparum in treated malaria patients by real-time PCR and high resolution melt analysis of genetic diversity. Sci Rep. 2018;8:10097.PubMedPubMedCentralCrossRef
74.
go back to reference Juliano JJ, Ariey F, Sem R, Tangpukdee N, Krudsood S, Olson C, et al. Misclassification of drug failure in Plasmodium falciparum clinical trials in southeast Asia. J Infect Dis. 2009;200:624–8.PubMedCrossRef Juliano JJ, Ariey F, Sem R, Tangpukdee N, Krudsood S, Olson C, et al. Misclassification of drug failure in Plasmodium falciparum clinical trials in southeast Asia. J Infect Dis. 2009;200:624–8.PubMedCrossRef
75.
go back to reference Su X, Wellems TE. Toward a high-resolution Plasmodium falciparum linkage map: polymorphic markers from hundreds of simple sequence repeats. Genomics. 1996;33:430–44.PubMedCrossRef Su X, Wellems TE. Toward a high-resolution Plasmodium falciparum linkage map: polymorphic markers from hundreds of simple sequence repeats. Genomics. 1996;33:430–44.PubMedCrossRef
76.
go back to reference Anderson TJ, Su XZ, Bockarie M, Lagog M, Day KP. Twelve microsatellite markers for characterization of Plasmodium falciparum from finger-prick blood samples. Parasitology. 1999;119(Pt 2):113–25.PubMedCrossRef Anderson TJ, Su XZ, Bockarie M, Lagog M, Day KP. Twelve microsatellite markers for characterization of Plasmodium falciparum from finger-prick blood samples. Parasitology. 1999;119(Pt 2):113–25.PubMedCrossRef
77.
go back to reference Wei G, Zhang L, Yan H, Zhao Y, Hu J, Pan W. Evaluation of the population structure and genetic diversity of Plasmodium falciparum in southern China. Malar J. 2015;14:283.PubMedPubMedCentralCrossRef Wei G, Zhang L, Yan H, Zhao Y, Hu J, Pan W. Evaluation of the population structure and genetic diversity of Plasmodium falciparum in southern China. Malar J. 2015;14:283.PubMedPubMedCentralCrossRef
78.
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.PubMedPubMedCentralCrossRef 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.PubMedPubMedCentralCrossRef
79.
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
80.
go back to reference Distefano G, Caruso M, La Malfa S, Gentile A, Wu SB. High resolution melting analysis is a more sensitive and effective alternative to gel-based platforms in analysis of SSR—an example in citrus. PLoS ONE. 2012;7:e44202.PubMedPubMedCentralCrossRef Distefano G, Caruso M, La Malfa S, Gentile A, Wu SB. High resolution melting analysis is a more sensitive and effective alternative to gel-based platforms in analysis of SSR—an example in citrus. PLoS ONE. 2012;7:e44202.PubMedPubMedCentralCrossRef
81.
go back to reference Tripathi M, Das A. Genotyping malaria parasites with DNA barcodes. Trop Med Int Health. 2015;20:1636–8.PubMedCrossRef Tripathi M, Das A. Genotyping malaria parasites with DNA barcodes. Trop Med Int Health. 2015;20:1636–8.PubMedCrossRef
82.
go back to reference Daniels R, Volkman SK, Milner DA, Mahesh N, Neafsey DE, Park DJ, et al. A general SNP-based molecular barcode for Plasmodium falciparum identification and tracking. Malar J. 2008;7:223.PubMedPubMedCentralCrossRef Daniels R, Volkman SK, Milner DA, Mahesh N, Neafsey DE, Park DJ, et al. A general SNP-based molecular barcode for Plasmodium falciparum identification and tracking. Malar J. 2008;7:223.PubMedPubMedCentralCrossRef
83.
go back to reference Searle KM, Katowa B, Kobayashi T, Siame MNS, Mharakurwa S, Carpi G, et al. Distinct parasite populations infect individuals identified through passive and active case detection in a region of declining malaria transmission in southern Zambia. Malar J. 2017;16:154.PubMedPubMedCentralCrossRef Searle KM, Katowa B, Kobayashi T, Siame MNS, Mharakurwa S, Carpi G, et al. Distinct parasite populations infect individuals identified through passive and active case detection in a region of declining malaria transmission in southern Zambia. Malar J. 2017;16:154.PubMedPubMedCentralCrossRef
84.
go back to reference Obaldia N 3rd, Baro NK, Calzada JE, Santamaria AM, Daniels R, Wong W, et al. Clonal outbreak of Plasmodium falciparum infection in eastern Panama. J Infect Dis. 2015;211:1087–96.PubMedCrossRef Obaldia N 3rd, Baro NK, Calzada JE, Santamaria AM, Daniels R, Wong W, et al. Clonal outbreak of Plasmodium falciparum infection in eastern Panama. J Infect Dis. 2015;211:1087–96.PubMedCrossRef
85.
go back to reference Campino S, Auburn S, Kivinen K, Zongo I, Ouedraogo JB, Mangano V, et al. Population genetic analysis of Plasmodium falciparum parasites using a customized Illumina GoldenGate genotyping assay. PLoS ONE. 2011;6:e20251.PubMedPubMedCentralCrossRef Campino S, Auburn S, Kivinen K, Zongo I, Ouedraogo JB, Mangano V, et al. Population genetic analysis of Plasmodium falciparum parasites using a customized Illumina GoldenGate genotyping assay. PLoS ONE. 2011;6:e20251.PubMedPubMedCentralCrossRef
86.
go back to reference Daniels RF, Schaffner SF, Wenger EA, Proctor JL, Chang HH, 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 HH, Wong W, et al. Modeling malaria genomics reveals transmission decline and rebound in Senegal. Proc Natl Acad Sci USA. 2015;112:7067–72.PubMedCrossRefPubMedCentral
87.
go back to reference Preston MD, Campino S, Assefa SA, Echeverry DF, Ocholla H, Amambua-Ngwa A, et al. A barcode of organellar genome polymorphisms identifies the geographic origin of Plasmodium falciparum strains. Nat Commun. 2014;5:4052.PubMedCrossRef Preston MD, Campino S, Assefa SA, Echeverry DF, Ocholla H, Amambua-Ngwa A, et al. A barcode of organellar genome polymorphisms identifies the geographic origin of Plasmodium falciparum strains. Nat Commun. 2014;5:4052.PubMedCrossRef
88.
go back to reference Pholwat S, Liu J, Stroup S, Jacob ST, Banura P, Moore CC, et al. The malaria TaqMan array card includes 87 assays for Plasmodium falciparum drug resistance, identification of species, and genotyping in a single reaction. Antimicrob Agents Chemother. 2017;61:e00110–7.PubMedPubMedCentralCrossRef Pholwat S, Liu J, Stroup S, Jacob ST, Banura P, Moore CC, et al. The malaria TaqMan array card includes 87 assays for Plasmodium falciparum drug resistance, identification of species, and genotyping in a single reaction. Antimicrob Agents Chemother. 2017;61:e00110–7.PubMedPubMedCentralCrossRef
89.
go back to reference Chang HH, Worby CJ, Yeka A, Nankabirwa J, Kamya MR, Staedke SG, et al. THE REAL McCOIL: a method for the concurrent estimation of the complexity of infection and SNP allele frequency for malaria parasites. PLoS Comput Biol. 2017;13:e1005348.PubMedPubMedCentralCrossRef Chang HH, Worby CJ, Yeka A, Nankabirwa J, Kamya MR, Staedke SG, et al. THE REAL McCOIL: a method for the concurrent estimation of the complexity of infection and SNP allele frequency for malaria parasites. PLoS Comput Biol. 2017;13:e1005348.PubMedPubMedCentralCrossRef
90.
go back to reference Nag S, Dalgaard MD, Kofoed PE, Ursing J, Crespo M, Andersen LO, et al. High throughput resistance profiling of Plasmodium falciparum infections based on custom dual indexing and Illumina next generation sequencing-technology. Sci Rep. 2017;7:2398.PubMedPubMedCentralCrossRef Nag S, Dalgaard MD, Kofoed PE, Ursing J, Crespo M, Andersen LO, et al. High throughput resistance profiling of Plasmodium falciparum infections based on custom dual indexing and Illumina next generation sequencing-technology. Sci Rep. 2017;7:2398.PubMedPubMedCentralCrossRef
91.
go back to reference Talundzic E, Ndiaye YD, Deme AB, Olsen C, Patel DS, Biliya S, et al. Molecular epidemiology of Plasmodium falciparum kelch13 mutations in Senegal determined by using targeted amplicon deep sequencing. Antimicrob Agents Chemother. 2017;61:e02116-16.PubMedPubMedCentralCrossRef Talundzic E, Ndiaye YD, Deme AB, Olsen C, Patel DS, Biliya S, et al. Molecular epidemiology of Plasmodium falciparum kelch13 mutations in Senegal determined by using targeted amplicon deep sequencing. Antimicrob Agents Chemother. 2017;61:e02116-16.PubMedPubMedCentralCrossRef
92.
go back to reference Anderson TJ, Nair S, McDew-White M, Cheeseman IH, Nkhoma S, Bilgic F, et al. Population parameters underlying an ongoing soft sweep in Southeast Asian malaria parasites. Mol Biol Evol. 2017;34:131–44.PubMedCrossRef Anderson TJ, Nair S, McDew-White M, Cheeseman IH, Nkhoma S, Bilgic F, et al. Population parameters underlying an ongoing soft sweep in Southeast Asian malaria parasites. Mol Biol Evol. 2017;34:131–44.PubMedCrossRef
93.
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;18:864.PubMedPubMedCentralCrossRef 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;18:864.PubMedPubMedCentralCrossRef
94.
go back to reference Neafsey DE, Juraska M, Bedford T, Benkeser D, Valim C, Griggs A, et al. Genetic diversity and protective efficacy of the RTS, S/AS01 malaria vaccine. N Engl J Med. 2015;373:2025–37.PubMedPubMedCentralCrossRef Neafsey DE, Juraska M, Bedford T, Benkeser D, Valim C, Griggs A, et al. Genetic diversity and protective efficacy of the RTS, S/AS01 malaria vaccine. N Engl J Med. 2015;373:2025–37.PubMedPubMedCentralCrossRef
95.
go back to reference Lo E, Zhou G, Oo W, Lee MC, Baum E, Felgner PL, et al. Molecular inference of sources and spreading patterns of Plasmodium falciparum malaria parasites in internally displaced persons settlements in Myanmar-China border area. Infect Genet Evol. 2015;33:189–96.PubMedPubMedCentralCrossRef Lo E, Zhou G, Oo W, Lee MC, Baum E, Felgner PL, et al. Molecular inference of sources and spreading patterns of Plasmodium falciparum malaria parasites in internally displaced persons settlements in Myanmar-China border area. Infect Genet Evol. 2015;33:189–96.PubMedPubMedCentralCrossRef
96.
go back to reference Okombo J, Kamau AW, Marsh K, Sutherland CJ, Ochola-Oyier LI. Temporal trends in prevalence of Plasmodium falciparum drug resistance alleles over two decades of changing antimalarial policy in coastal Kenya. Int J Parasitol Drugs Drug Resist. 2014;4:152–63.PubMedPubMedCentralCrossRef Okombo J, Kamau AW, Marsh K, Sutherland CJ, Ochola-Oyier LI. Temporal trends in prevalence of Plasmodium falciparum drug resistance alleles over two decades of changing antimalarial policy in coastal Kenya. Int J Parasitol Drugs Drug Resist. 2014;4:152–63.PubMedPubMedCentralCrossRef
97.
go back to reference Bousema T, Griffin JT, Sauerwein RW, Smith DL, Churcher TS, Takken W, et al. Hitting hotspots: spatial targeting of malaria for control and elimination. PLoS Med. 2012;9:e1001165.PubMedPubMedCentralCrossRef Bousema T, Griffin JT, Sauerwein RW, Smith DL, Churcher TS, Takken W, et al. Hitting hotspots: spatial targeting of malaria for control and elimination. PLoS Med. 2012;9:e1001165.PubMedPubMedCentralCrossRef
98.
go back to reference Griffin JT, Hollingsworth TD, Okell LC, Churcher TS, White M, et al. Reducing Plasmodium falciparum malaria transmission in Africa: a model-based evaluation of intervention strategies. PLoS Med. 2010;7:e1000324.PubMedPubMedCentralCrossRef Griffin JT, Hollingsworth TD, Okell LC, Churcher TS, White M, et al. Reducing Plasmodium falciparum malaria transmission in Africa: a model-based evaluation of intervention strategies. PLoS Med. 2010;7:e1000324.PubMedPubMedCentralCrossRef
99.
go back to reference Wong W, Griggs AD, Daniels RF, Schaffner SF, Ndiaye D, Bei AK, et al. Genetic relatedness analysis reveals the cotransmission of genetically related Plasmodium falciparum parasites in Thies, Senegal. Genome Med. 2017;9:5.PubMedPubMedCentralCrossRef Wong W, Griggs AD, Daniels RF, Schaffner SF, Ndiaye D, Bei AK, et al. Genetic relatedness analysis reveals the cotransmission of genetically related Plasmodium falciparum parasites in Thies, Senegal. Genome Med. 2017;9:5.PubMedPubMedCentralCrossRef
100.
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
Metadata
Title
Genetic diversity and drug resistance surveillance of Plasmodium falciparum for malaria elimination: is there an ideal tool for resource-limited sub-Saharan Africa?
Authors
Tobias O. Apinjoh
Amed Ouattara
Vincent P. K. Titanji
Abdoulaye Djimde
Alfred Amambua-Ngwa
Publication date
01-12-2019
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2019
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-019-2844-5

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