Contrasting genomic epidemiology between sympatric Plasmodium falciparum and Plasmodium vivax populations.
Humans
Plasmodium vivax
/ genetics
Plasmodium falciparum
/ genetics
Malaria, Vivax
/ epidemiology
Malaria, Falciparum
/ epidemiology
Adult
Male
Female
Sympatry
Middle Aged
Young Adult
Adolescent
Genomics
/ methods
Genome, Protozoan
/ genetics
Child
Child, Preschool
Genetic Variation
Molecular Epidemiology
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
30 Sep 2024
30 Sep 2024
Historique:
received:
11
04
2024
accepted:
11
09
2024
medline:
1
10
2024
pubmed:
1
10
2024
entrez:
30
9
2024
Statut:
epublish
Résumé
The malaria parasites Plasmodium falciparum and Plasmodium vivax differ in key biological processes and associated clinical effects, but consequences on population-level transmission dynamics are difficult to predict. This co-endemic malaria study from Guyana details important epidemiological contrasts between the species by coupling population genomics (1396 spatiotemporally matched parasite genomes, primarily from 2020-21) with sociodemographic analysis (nationwide patient census from 2019). We describe how P. falciparum forms large, interrelated subpopulations that sporadically expand but generally exhibit restrained dispersal, whereby spatial distance and patient travel statistics predict parasite identity-by-descent (IBD). Case bias towards working-age adults is also strongly pronounced. P. vivax exhibits 46% higher average nucleotide diversity (π) and 6.5x lower average IBD. It occupies a wider geographic range, without evidence for outbreak-like expansions, only microgeographic patterns of isolation-by-distance, and weaker case bias towards adults. Possible latency-relapse effects also manifest in various analyses. For example, 11.0% of patients diagnosed with P. vivax in Greater Georgetown report no recent travel to endemic zones, and P. vivax clones recur in 11 of 46 patients incidentally sampled twice during the study. Polyclonality rate is also 2.1x higher than in P. falciparum, does not trend positively with estimated incidence, and correlates uniquely to selected demographics. We discuss possible underlying mechanisms and implications for malaria control.
Identifiants
pubmed: 39349478
doi: 10.1038/s41467-024-52545-6
pii: 10.1038/s41467-024-52545-6
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
8450Subventions
Organisme : Bill & Melinda Gates Foundation
ID : INV-009416
Pays : United States
Organisme : U.S. Department of Health & Human Services | NIH | National Institute of Allergy and Infectious Diseases (NIAID)
ID : U19AI110818
Organisme : U.S. Department of Health & Human Services | NIH | National Institute of Allergy and Infectious Diseases (NIAID)
ID : U19AI110818
Organisme : Scottish Funding Council (SFC)
ID : SFC/AN/12/2017
Organisme : Scottish Funding Council (SFC)
ID : SFC/AN/12/2017
Organisme : RCUK | Engineering and Physical Sciences Research Council (EPSRC)
ID : EP/T003782/1
Organisme : RCUK | Engineering and Physical Sciences Research Council (EPSRC)
ID : EP/T003782/1
Informations de copyright
© 2024. The Author(s).
Références
World Health Organization. WHO Malaria Report 2023 (WHO, 2023).
Weiss, D. J. et al. Mapping the global prevalence, incidence, and mortality of Plasmodium falciparum, 2000-17: a spatial and temporal modelling study. Lancet Lond. Engl. 394, 322–331 (2019).
doi: 10.1016/S0140-6736(19)31097-9
Battle, K. E. et al. Mapping the global endemicity and clinical burden of Plasmodium vivax, 2000-17: a spatial and temporal modelling study. Lancet Lond. Engl. 394, 332–343 (2019).
doi: 10.1016/S0140-6736(19)31096-7
Price, R. N., Commons, R. J., Battle, K. E., Thriemer, K. & Mendis, K. Plasmodium vivax in the era of the shrinking P. falciparum map. Trends Parasitol. 36, 560–570 (2020).
pmcid: 7297627
doi: 10.1016/j.pt.2020.03.009
Oliveira-Ferreira, J. et al. Malaria in Brazil: an overview. Malar. J. 9, 115 (2010).
pmcid: 2891813
doi: 10.1186/1475-2875-9-115
Rosas-Aguirre, A. et al. Epidemiology of Plasmodium vivax malaria in Peru. Am. J. Trop. Med. Hyg. 95, 133–144 (2016).
pmcid: 5201219
doi: 10.4269/ajtmh.16-0268
Sattabongkot, J., Tsuboi, T., Zollner, G. E., Sirichaisinthop, J. & Cui, L. Plasmodium vivax transmission: chances for control? Trends Parasitol. 20, 192–198 (2004).
doi: 10.1016/j.pt.2004.02.001
Sattabongkot, J. et al. Malaria research for tailored control and elimination strategies in the greater Mekong subregion. Am. J. Trop. Med. Hyg. 107, 152–159 (2022).
pmcid: 9662225
doi: 10.4269/ajtmh.21-1268
Kenangalem, E. et al. Malaria morbidity and mortality following introduction of a universal policy of artemisinin-based treatment for malaria in Papua, Indonesia: a longitudinal surveillance study. PLoS Med. 16, e100281510 (2019).
doi: 10.1371/journal.pmed.1002815
Sharp, P. M., Plenderleith, L. J. & Hahn, B. H. Ape origins of human malaria. Annu. Rev. Microbiol. 74, 39–63 (2020).
pmcid: 7643433
doi: 10.1146/annurev-micro-020518-115628
Cepeda, A. S. et al. The genome of Plasmodium gonderi: insights into the evolution of human malaria parasites. Genome Biol. Evol. 16, evae027 (2024).
Cowman, A. F., Healer, J., Marapana, D. & Marsh, K. Malaria: biology and disease. Cell 167, 610–624 (2016).
doi: 10.1016/j.cell.2016.07.055
Krotoski, W. A. et al. Demonstration of hypnozoites in sporozoite-transmitted Plasmodium vivax infection. Am. J. Trop. Med. Hyg. 31, 1291–1293 (1982).
doi: 10.4269/ajtmh.1982.31.1291
Llanos-Cuentas, A. et al. Tafenoquine versus primaquine to prevent relapse of Plasmodium vivax malaria. N. Engl. J. Med. 380, 229–241 (2019).
pmcid: 6657225
doi: 10.1056/NEJMoa1802537
Recht, J., Ashley, E. A. & White, N. J. Use of primaquine and glucose-6-phosphate dehydrogenase deficiency testing: divergent policies and practices in malaria endemic countries. PLoS Negl. Trop. Dis. 12, e0006230 (2018).
pmcid: 5908060
doi: 10.1371/journal.pntd.0006230
Bruxvoort, K., Goodman, C., Kachur, S. P. & Schellenberg, D. How patients take malaria treatment: a systematic review of the literature on adherence to antimalarial drugs. PloS One 9, e84555 (2014).
pmcid: 3896377
doi: 10.1371/journal.pone.0084555
Craik, R. A note on the erythrocytes in malaria. Lancet 195, 1110 (1920).
doi: 10.1016/S0140-6736(00)92210-4
Cheng, Q., Cunningham, J. & Gatton, M. L. Systematic review of sub-microscopic P. vivax infections: prevalence and determining factors. PLoS Negl. Trop. Dis. 9, e3413 (2015).
pmcid: 4288718
doi: 10.1371/journal.pntd.0003413
Boyd, M. F. & Kitchen, S. F. On the infectiousness of patients infected with Plasmodium vivax and Plasmodium falciparum. Am. J. Trop. Med. Hyg. s1-17, 253–262 (1937).
doi: 10.4269/ajtmh.1937.s1-17.253
Wernsdorfer, W. H. Malaria: Principles and Practice of Malariology. Vol. 2092 (Edinburgh; New York, 1988).
Boyd, M. F., Stratman-Thomas, W. K. & Kitchen, S. F. On the relative susceptibility of Anopheles quadrimaculatus to Plasmodium vivax and Plasmodium falciparum. Am. J. Trop. Med. Hyg. s1-15, 485–493 (1935).
doi: 10.4269/ajtmh.1935.s1-15.485
Boyd, M. F., Stratman-Thomas, W. K. & Muench, H. The occurrence of gametocytes of Plasmodium vivax during the primary attack. Am. J. Trop. Med. Hyg. s1-16, 133–138 (1936).
doi: 10.4269/ajtmh.1936.s1-16.133
Pukrittayakamee, S. et al. Effects of different antimalarial drugs on gametocyte carriage in P. vivax malaria. Am. J. Trop. Med. Hyg. 79, 378–384 (2008).
doi: 10.4269/ajtmh.2008.79.378
Galinski, M. R., Meyer, E. V. S. & Barnwell, J. W. Plasmodium vivax: modern strategies to study a persistent parasite’s life cycle. In: Advances in Parasitology Vol. 81 (eds. Hay, S. I., Price, R. & Baird, J. K.) 1–26 (Academic Press, 2013).
Timinao, L. et al. Infectivity of symptomatic malaria patients to Anopheles farauti colony mosquitoes in Papua new Guinea. Front. Cell. Infect. Microbiol. 11, 771233 (2021).
pmcid: 8729879
doi: 10.3389/fcimb.2021.771233
Blackburn, D. et al. Outbreak of locally acquired mosquito-transmitted (autochthonous) malaria — Florida and Texas, May–July 2023. Morb. Mortal. Wkly. Rep. 72, 973–978 (2023).
doi: 10.15585/mmwr.mm7236a1
Danis, K. et al. Malaria in Greece: historical and current reflections on a re-emerging vector borne disease. Travel Med. Infect. Dis. 11, 8–14 (2013).
doi: 10.1016/j.tmaid.2013.01.001
Bahk, Y. Y. et al. Epidemiological characteristics of re-emerging vivax malaria in the republic of Korea (1993–2017). Korean J. Parasitol. 56, 531–543 (2018).
pmcid: 6327199
doi: 10.3347/kjp.2018.56.6.531
Lopez, L. & Koepfli, C. Systematic review of Plasmodium falciparum and Plasmodium vivax polyclonal infections: impact of prevalence, study population characteristics, and laboratory procedures. PLoS ONE 16, e0249382 (2021).
pmcid: 8195386
doi: 10.1371/journal.pone.0249382
De Salazar, P. M., Cox, H., Imhoff, H., Alexandre, J. S. F. & Buckee, C. O. The association between gold mining and malaria in Guyana: a statistical inference and time-series analysis. Lancet Planet. Health 5, e731–e738 (2021).
pmcid: 8515511
doi: 10.1016/S2542-5196(21)00203-5
Howes, R. E. et al. Plasmodium vivax transmission in Africa. PLoS Negl. Trop. Dis. 9, e0004222 (2015).
pmcid: 4654493
doi: 10.1371/journal.pntd.0004222
Olapeju, B. et al. Malaria prevention and care seeking among gold miners in Guyana. PloS ONE 15, e0244454 (2020).
pmcid: 7771697
doi: 10.1371/journal.pone.0244454
Hilson, G. & Laing, T. Gold mining, indigenous land claims and conflict in Guyana’s hinterland. J. Rural Stud. 50, 172–187 (2017).
doi: 10.1016/j.jrurstud.2017.01.004
Neafsey, D. E. et al. The malaria parasite Plasmodium vivax exhibits greater genetic diversity than Plasmodium falciparum. Nat. Genet. 44, 1046–1050 (2012).
pmcid: 3432710
doi: 10.1038/ng.2373
Schaffner, D. F., Taylor, A. R., Wong, W., Wirth, D. F. & Neafsey, D. E. hmmIBD: software to infer pairwise identity by descent between haploid genotypes. Malar. J. 17, 196 (2018).
pmcid: 5952413
doi: 10.1186/s12936-018-2349-7
Chang, H. H. 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. 13, e1005348 (2017).
Vanhove, M. et al. Temporal and spatial dynamics of Plasmodium falciparum clonal lineages in Guyana. PLoS Pathog. 20, e1012013 (2024).
Hubbard, A. et al. Implementing landscape genetics in molecular epidemiology to determine drivers of vector-borne disease: a malaria case study. Mol. Ecol. 32, 1848–1859 (2023).
pmcid: 10694861
doi: 10.1111/mec.16846
Verity, R. et al. The impact of antimalarial resistance on the genetic structure of Plasmodium falciparum in the DRC. Nat. Commun. 11, 2107 (2020).
pmcid: 7192906
doi: 10.1038/s41467-020-15779-8
Tessema, S. et al. Using parasite genetic and human mobility data to infer local and cross-border malaria connectivity in Southern Africa. eLife 8, e43510 (2019).
pmcid: 6478435
doi: 10.7554/eLife.43510
Popovici, J. et al. Genomic analyses reveal the common occurrence and complexity of Plasmodium vivax relapses in Cambodia. mBio 9, e01888–17 (2018).
Manzoni, G. et al. Progress towards malaria elimination in the Greater Mekong Subregion: perspectives from the World Health Organization. Malar. J. 23, 64 (2024).
pmcid: 10908136
doi: 10.1186/s12936-024-04851-z
Douine, M. et al. Malakit: an innovative pilot project to self-diagnose and self-treat malaria among illegal gold miners in the Guiana shield. Malar. J. 17, 158 (2018).
pmcid: 5892004
doi: 10.1186/s12936-018-2306-5
Douine, M. et al. Self-diagnosis and self-treatment of malaria in hard-to-reach and mobile populations of the Amazon: results of Malakit, an international multicentric intervention research project. Lancet Reg. Health Am. 4, 100047 (2021).
pmcid: 9903903
Thriemer, K., Ley, B. & von Seidlein, L. Towards the elimination of Plasmodium vivax malaria: implementing the radical cure. PLoS Med. 18, e1003494 (2021).
pmcid: 8064598
doi: 10.1371/journal.pmed.1003494
Sanna, A. et al. CUREMA project: a further step towards malaria elimination among hard-to-reach and mobile populations. Malar. J. 23, 271 (2024).
Thriemer, K. et al. Primaquine radical cure in patients with Plasmodium falciparum malaria in areas co-endemic for P. falciparum and Plasmodium vivax (PRIMA): a multicentre, open-label, superiority randomised controlled trial. Lancet Lond. Engl. 402, 2101–2110 (2023).
doi: 10.1016/S0140-6736(23)01553-2
Lopes-Rafegas, I., Cox, H., Mora, T. & Sicuri, E. The contribution of risk perception and social norms to reported preventive behaviour against selected vector-borne diseases in Guyana. Sci. Rep. 13, 16866 (2023).
pmcid: 10558444
doi: 10.1038/s41598-023-43991-1
Gerlovina, I., Gerlovin, B., Rodríguez-Barraquer, I. & Greenhouse, B. Dcifer: an IBD-based method to calculate genetic distance between polyclonal infections. Genetics 222, iyac126 (2022).
pmcid: 9526043
doi: 10.1093/genetics/iyac126
Tyers, M. riverdist: river network distance computation and applications. R package version 0.16.3 (2024).
van Etten, J., de Sousa, K. & Marx, A. gdistance: distances and routes on geographical grids. R package version 1.6.4 (2023).
QGIS Development Team. Open Source Geospatial Foundation. Software version 2.18.4 (2017).
Rose, A. et al. LandScan Global 2019. Oak Ridge National Laboratory, Oak Ridge, TN (2020).
Oyola, S. O. et al. Whole genome sequencing of Plasmodium falciparum from dried blood spots using selective whole genome amplification. Malar. J. 15, 597 (2016).
pmcid: 5175302
doi: 10.1186/s12936-016-1641-7
Cowell, A. N. et al. Selective whole-genome amplification Is a robust method that enables scalable whole-genome sequencing of Plasmodium vivax from unprocessed clinical samples. mBio 8, e02257–16 (2017).
Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25, 1754–1760 (2009).
pmcid: 2705234
doi: 10.1093/bioinformatics/btp324
McKenna, A. et al. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20, 1297–1303 (2010).
pmcid: 2928508
doi: 10.1101/gr.107524.110
Miles, A. et al. Indels, structural variation, and recombination drive genomic diversity in Plasmodium falciparum. Genome Res. 26, 1288–1299 (2016).
pmcid: 5052046
doi: 10.1101/gr.203711.115
de Oliveira, T. C. et al. Population genomics reveals the expansion of highly inbred Plasmodium vivax lineages in the main malaria hotspot of Brazil. PLoS Negl. Trop. Dis. 14, e0008808 (2020).
pmcid: 7592762
doi: 10.1371/journal.pntd.0008808
Danecek, P. et al. The variant call format and VCFtools. Bioinformatics 27, 2156–2158 (2011).
pmcid: 3137218
doi: 10.1093/bioinformatics/btr330
Purcell, S. et al. PLINK: A tool set for whole-genome association and population-based linkage analyses. Am. J. Hum. Genet. 81, 559–575 (2007).
pmcid: 1950838
doi: 10.1086/519795
Csárdi, G. et al. igraph for R: R interface of the igraph library for graph theory and network analysis. R package version 1.3.5 (2022).
Oksanen, J. et al. Vegan: community ecology package. R package version 2.6-4 (2022).
GADM. Database of Global Administrative Areas version 4.1 (2018).