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Genetic diversity of Plasmodium vivax over time and space: a community-based study in rural Amazonia

Published online by Cambridge University Press:  28 July 2014

CAMILLA L. BATISTA
Affiliation:
Department of Parasitology, Institute of Biomedical Sciences, University of São Paulo, Av. Prof. Lineu Prestes 1374, 05508-900 São Paulo, SP, Brazil
SUSANA BARBOSA
Affiliation:
Department of Parasitology, Institute of Biomedical Sciences, University of São Paulo, Av. Prof. Lineu Prestes 1374, 05508-900 São Paulo, SP, Brazil
MELISSA DA SILVA BASTOS
Affiliation:
Department of Parasitology, Institute of Biomedical Sciences, University of São Paulo, Av. Prof. Lineu Prestes 1374, 05508-900 São Paulo, SP, Brazil
SUSANA ARIANE S. VIANA
Affiliation:
Department of Parasitology, Institute of Biomedical Sciences, University of São Paulo, Av. Prof. Lineu Prestes 1374, 05508-900 São Paulo, SP, Brazil
MARCELO U. FERREIRA*
Affiliation:
Department of Parasitology, Institute of Biomedical Sciences, University of São Paulo, Av. Prof. Lineu Prestes 1374, 05508-900 São Paulo, SP, Brazil
*
*Corresponding author: Department of Parasitology, Institute of Biomedical Sciences, University of São Paulo, Av. Prof. Lineu Prestes 1374, 05508-900 São Paulo, SP, Brazil. E-mail: muferrei@usp.br

Summary

To examine how community-level genetic diversity of the malaria parasite Plasmodium vivax varies across time and space, we investigated the dynamics of parasite polymorphisms during the early phases of occupation of a frontier settlement in the Amazon Basin of Brazil. Microsatellite characterization of 84 isolates of P. vivax sampled over 3 years revealed a moderate-to-high genetic diversity (mean expected heterozygosity, 0·699), with a large proportion (78·5%) of multiple-clone infections (MCI), but also a strong multilocus linkage disequilibrium (LD) consistent with rare outcrossing. Little temporal and no spatial clustering was observed in the distribution of parasite haplotypes. A single microsatellite haplotype was shared by 3 parasites collected during an outbreak; all other 81 haplotypes were recovered only once. The lowest parasite diversity, with the smallest proportion of MCI and the strongest LD, was observed at the time of the outbreak, providing a clear example of epidemic population structure in a human pathogen. Population genetic parameters returned to pre-outbreak values during last 2 years of study, despite the concomitant decline in malaria incidence. We suggest that parasite genotyping can be useful for tracking the spread of new parasite strains associated with outbreaks in areas approaching malaria elimination.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2014 

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References

REFERENCES

Anderson, T. J. C., Haubold, B., Williams, J. T., Estrada-Franco, J. G., Richardson, L., Mollinedo, R., Bockarie, M., Mokili, J., Mharakurwa, S., French, N., Whitworth, J., Velez, I. D., Brockman, A. H., Nosten, F., Ferreira, M. U. and Day, K. P. (2000). Microsatellite markers reveal a spectrum of population structures in the malaria parasite Plasmodium falciparum . Molecular Biology and Evolution 17, 14671482.CrossRefGoogle ScholarPubMed
Battle, K. E., Gething, P. W., Elyazar, I. R., Moyes, C. L., Sinka, M. E., Howes, R. E., Guerra, C. A., Price, R. N., Baird, K. J. and Hay, S. I. (2012). The global public health significance of Plasmodium vivax . Advances in Parasitology 8, 1111. doi: 10.1016/B978-0-12-397900-1.00001-3.Google Scholar
Bell, A. S., de Roode, J. C., Sim, D. and Read, A. F. (2006). Within-host competition in genetically diverse malaria infections: parasite virulence and competitive success. Evolution 60, 13581371.Google ScholarPubMed
Castro, M. C., Monte-Mór, R. L., Sawyer, D. O. and Singer, B. H. (2006). Malaria risk on the Amazon frontier. Proceedings of the National Academy of Sciences, USA 103, 24522457.CrossRefGoogle ScholarPubMed
Charlesworth, B. and Charlesworth, D. (1975). An experiment on recombination load in Drosophila melanogaster . Genetics Research 25, 267274.CrossRefGoogle Scholar
Chenet, S. M., Schneider, K. A., Villegas, L. and Escalante, A. A. (2012). Local population structure of Plasmodium: impact on malaria control and elimination. Malaria Journal 11, 412. doi: 10.1186/1475-2875-11-412.CrossRefGoogle ScholarPubMed
Daniels, R., Volkman, S. K., Milner, D. A., Mahesh, N., Neafsey, D. E., Park, D. J., Rosen, D., Angelino, E., Sabeti, P. C., Wirth, D. F. and Wiegand, R. C. (2008). A general SNP-based molecular barcode for Plasmodium falciparum identification and tracking. Malaria Journal 7, 223. doi: 10.1186/1475-2875-7-223.CrossRefGoogle ScholarPubMed
da Silva-Nunes, M. and Ferreira, M. U. (2007). Clinical spectrum of uncomplicated malaria in semi-immune Amazonians: beyond the ‘symptomatic’ vs ‘asymptomatic’ dichotomy. Memórias do Instituto Oswaldo Cruz 102, 341347.CrossRefGoogle ScholarPubMed
da Silva-Nunes, M., Codeço, C. T., Malafronte, R. S., da Silva, N. S., Juncansen, C., Muniz, P. T. and Ferreira, M. U. (2008). Malaria on the Amazonian frontier: transmission dynamics, risk factors, spatial distribution, and prospects for control. American Journal of Tropical Medicine and Hygiene 79, 624635.CrossRefGoogle ScholarPubMed
da Silva-Nunes, M., Moreno, M., Conn, J. E., Gamboa, D., Abeles, S., Vinetz, J. M. and Ferreira, M. U. (2012). Amazonian malaria: asymptomatic human reservoirs, diagnostic challenges, environmentally driven changes in mosquito vector populations, and the mandate for sustainable control strategies. Acta Tropica 121, 281291. doi: 10.1016/j.actatropica.2011.10.001.CrossRefGoogle ScholarPubMed
de Roode, J. C., Pansini, R., Cheesman, S. J., Helinski, M. E., Huijben, S., Wargo, A. R., Bell, A. S., Chan, B. H., Walliker, D. and Read, A. F. (2005). Virulence and competitive ability in genetically diverse malaria infections. Proceedings of the National Academy of Sciences, USA 102, 76247628.CrossRefGoogle ScholarPubMed
Dorken, M. E. and Eckert, C. G. (2001). Severely reduced sexual reproduction in northern populations of a clonal plant, Decoden verticullatus (Lynthraceae). Journal of Ecology 89, 339350.CrossRefGoogle Scholar
Farnert, A. (2008). Plasmodium falciparum population dynamics: only snapshots in time? Trends in Parasitology 24, 340344. doi: 10.1016/j.pt.2008.04.008.CrossRefGoogle ScholarPubMed
Feil, E. J., Li, B. C., Aanensen, D. M., Hanage, W. P. and Spratt, B. G. (2004). eBURST: inferring patterns of evolutionary descent among clusters of related bacterial genotypes from multilocus sequence typing data. Journal of Bacteriology 186, 15181530.CrossRefGoogle ScholarPubMed
Ferreira, M. U., Karunaweera, N. D., da Silva-Nunes, M., da Silva, N. S., Wirth, D. F. and Hartl, D. L. (2007). Population structure and transmission dynamics of Plasmodium vivax in rural Amazonia. Journal of Infectious Diseases 195, 12181226. doi: 10.1086/512685.CrossRefGoogle ScholarPubMed
Garza, J. C. and Williamson, E. G. (2001). Detection of reduction in population size using data from microsatellite loci. Molecular Ecology 10, 305318.CrossRefGoogle ScholarPubMed
Gething, P. W., Elyazar, I. R., Moyes, C. L., Smith, D. L., Battle, K. E., Guerra, C. A., Patil, A. P., Tatem, A. J., Howes, R. E., Myers, M. F., George, D. B., Horby, P., Wertheim, H. F., Price, R. N., Mueller, I., Baird, J. K. and Hay, S. I. (2012). A long neglected world malaria map: Plasmodium vivax endemicity in 2010. PLoS Neglected Tropical Diseases 6, e1814. doi: 10.1371/journal.pntd.0001814.CrossRefGoogle ScholarPubMed
Gonçalves, R. M., Scopel, K. K. G., Bastos, M. S. and Ferreira, M. U. (2012). Cytokine balance in human malaria: does Plasmodium vivax elicit more inflammatory responses than Plasmodium falciparum? PLoS ONE 7, 44394. doi: 10.1371/journal.pone.0044394.CrossRefGoogle ScholarPubMed
Gunawardena, S., Karunaweera, N. D., Ferreira, M. U., Phone-Kyaw, M., Pollack, R. J., Alifrangis, M., Rajakaruna, R. S., Konradsen, F., Amerasinghe, P. H., Schousboe, M. L., Galappaththy, G. N., Abeyasinghe, R. R., Hartl, D. L. and Wirth, D. F. (2010). Geographic structure of Plasmodium vivax: microsatellite analysis of parasite populations from Sri Lanka, Myanmar, and Ethiopia. American Journal of Tropical Medicine and Hygiene 82, 235242. doi: 10.4269/ajtmh.2010.09-0588.CrossRefGoogle ScholarPubMed
Gunawardena, S., Ferreira, M. U., Kapilananda, G. M., Wirth, D. F. and Karunaweera, N. D. (2014). The Sri Lankan paradox: high genetic diversity in Plasmodium vivax populations despite decreasing levels of malaria transmission. Parasitology 141, 880890. doi: 10.1017/S0031182013002278.CrossRefGoogle ScholarPubMed
Haubold, B. and Hudson, R. R. (2000). LIAN 3.0: detecting linkage disequilibrium in multilocus data. Linkage analysis. Bioinformatics 16, 847848.CrossRefGoogle ScholarPubMed
Havryliuk, T. and Ferreira, M. U. (2009). A closer look at multiple-clone Plasmodium vivax infections: detection methods, prevalence and consequences. Memórias do Instituto Oswaldo Cruz 104, 6773.CrossRefGoogle Scholar
Havryliuk, T., Orjuela-Sánchez, P. and Ferreira, M. U. (2008). Plasmodium vivax: microsatellite analysis of multiple-clone infections. Experimental Parasitology 120, 330336. doi: 10.1016/j.exppara.2008.08.012.CrossRefGoogle ScholarPubMed
Imwong, M., Pukrittayakamee, S., Grüner, A. C., Rénia, L., Letourneur, F., Looareesuwan, S., White, N. J. and Snounou, G. (2005). Practical PCR genotyping protocols for Plasmodium vivax using Pvcs and Pvmsp1 . Malaria Journal 4, 20.CrossRefGoogle ScholarPubMed
Iwagami, M., Hwang, S. Y., Kim, S. H., Park, S. J., Lee, G. Y., Matsumoto-Takahashi, E. L., Kho, W. G. and Kano, S. (2013). Microsatellite DNA analysis revealed a drastic genetic change of Plasmodium vivax population in the Republic of Korea during 2002 and 2003. PLoS Neglected Tropical Diseases 7, e2522. doi: 10.1371/journal.pntd.0002522.CrossRefGoogle Scholar
Karunaweera, N. D., Ferreira, M. U., Hartl, D. L. and Wirth, D. F. (2007). Fourteen polymorphic microsatellite DNA markers for the human malaria parasite Plasmodium vivax . Molecular Ecology 7, 172175.CrossRefGoogle Scholar
Koepfli, C., Mueller, I., Marfurt, J., Goroti, M., Sie, A., Oa, O., Genton, B., Beck, H. P. and Felger, I. (2009). Evaluation of Plasmodium vivax genotyping markers for molecular monitoring in clinical trials. Journal of Infectious Diseases 19, 10741080. doi: 10.1086/597303.CrossRefGoogle Scholar
Koepfli, C., Timinao, L., Antao, T., Barry, A. E., Siba, P., Mueller, I. and Felger, I. (2013). A large Plasmodium vivax reservoir and little population structure in the South Pacific. PLoS ONE 18, e66041. doi: 10.1371/journal.pone.0066041.CrossRefGoogle Scholar
Luikart, G., Allendorf, F. W., Cornuet, J. M. and Sherwin, W. B. (1998). Distortion of allele frequency distributions provides a test for recent population bottlenecks. Journal of Heredity 89, 238247.CrossRefGoogle ScholarPubMed
Mantel, N. (1967). The detection of disease clustering and a generalized regression approach. Cancer Research 27, 209220.Google Scholar
Mideo, N. (2009). Parasite adaptations to within-host competition. Trends in Parasitology 25, 261268. doi: 10.1016/j.pt.2009.03.001.CrossRefGoogle ScholarPubMed
Ministry of Health of Brazil (2010). Practical Guidelines for Malaria Therapy [in Portuguese]. Ministry of Health of Brazil, Brasília. http://bvsms.saude.gov.br/bvs/publicacoes/guia_pratico_malaria.pdf.Google Scholar
Neafsey, D. E., Galinsky, K., Jiang, R. H., Young, L., Sykes, S. M., Saif, S., Gujja, S., Goldberg, J. M., Young, S., Zeng, Q., Chapman, S. B., Dash, A. P., Anvikar, A. R., Sutton, P. L., Birren, B. W., Escalante, A. A., Barnwell, J. W. and Carlton, J. M. (2012). The malaria parasite Plasmodium vivax exhibits greater genetic diversity than Plasmodium falciparum . Nature Genetics 44, 10461050. doi: 10.1038/ng.2373.CrossRefGoogle ScholarPubMed
Nkhoma, S. C., Nair, S., Al-Saai, S., Ashley, E., McGready, R., Phyo, A. P., Nosten, F. and Anderson, T. J. C. (2013). Population genetic correlates of declining transmission in a human pathogen. Molecular Ecology 22, 273285. doi: 10.1111/mec.12099.CrossRefGoogle Scholar
Norris, D. E. (2004). Mosquito-borne diseases as a consequence of land use change. EcoHealth 1, 1924.CrossRefGoogle Scholar
Orjuela-Sánchez, P., da Silva, N. S., da Silva-Nunes, M. and Ferreira, M. U. (2009). Recurrent parasitemias and population dynamics of Plasmodium vivax polymorphisms in rural Amazonia. American Journal of Tropical Medicine and Hygiene 81, 961968. doi: 10.4269/ajtmh.2009.09-0337.CrossRefGoogle ScholarPubMed
Orjuela-Sánchez, P., Karunaweera, N. D., da Silva-Nunes, M., da Silva, N. S., Scopel, K. K. G., Goncalves, R. M., Amaratunga, C., , J. M., Socheat, D., Fairhurst, R. M., Gunawardena, S., Thavakodirasah, T., Galapaththy, G. N. L., Abeysinghe, R. R., Kawamoto, F., Wirth, D. F. and Ferreira, M. U. (2010). Single-nucleotide polymorphism, linkage disequilibrium and geographic structure in the malaria parasite Plasmodium vivax: prospects for genome-wide association studies. BMC Genetics 11, 65. doi: 10.1186/1471-2156-11-65.CrossRefGoogle ScholarPubMed
Orjuela-Sánchez, P., Brandi, M. C. and Ferreira, M. U. (2013 a). Microsatellite analysis of malaria parasites. Methods in Molecular Biology 1006, 247258. doi: 10.1007/978-1-62703-389-3_17.CrossRefGoogle ScholarPubMed
Orjuela-Sánchez, P., , J. M., Brandi, M. C., Rodrigues, P. T., Bastos, M. S., Amaratunga, C., Duong, S., Fairhurst, R. M. and Ferreira, M. U. (2013 b). Higher microsatellite diversity in Plasmodium vivax than in sympatric Plasmodium falciparum populations in Pursat, Western Cambodia. Experimental Parasitology 134, 318326. doi: 10.1016/j.exppara.2013.03.029.CrossRefGoogle ScholarPubMed
Price, R. N., Tjitra, E., Guerra, C. A., Yeung, S., White, N. J. and Anstey, N. M. (2007). Vivax malaria: neglected and not benign. American Journal of Tropical Medicine and Hygiene 77(6 Suppl.), 7987.CrossRefGoogle Scholar
Pritchard, J. K., Stephens, M. and Donnelly, P. (2000). Inference of population structure using multilocus genotype data. Genetics 155, 945959.CrossRefGoogle ScholarPubMed
R Core Team (2013). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/ Google Scholar
Rezende, A. M., Tarazona-Santos, E., Fontes, C. J. F., Souza, J. M., Couto, A. D., Carvalho, L. H. and Brito, C. F. A. (2010). Microsatellite loci: determining the genetic variability of Plasmodium vivax . Tropical Medicine and International Health 15, 718726. doi: 10.1111/j.1365-3156.2010.02535.x.CrossRefGoogle ScholarPubMed
Sinka, M. E., Rubio-Palis, Y., Manguin, S., Patil, A. P., Temperley, W. H., Gething, P. W., Van Boeckel, T., Kabaria, C. W., Harbach, R. E. and Hay, S. I. (2010). The dominant Anopheles vectors of human malaria in the Americas: occurrence data, distribution maps and bionomic précis. Parasite and Vectors 3, 72. doi: 10.1186/1756-3305-5-69.CrossRefGoogle ScholarPubMed
Smith, J. M., Smith, N. H., O'rourke, M. and Spratt, B. G. (1993). How clonal are bacteria? Proceedings of the National Academy of Sciences, USA 90, 43844388.CrossRefGoogle ScholarPubMed
Sutton, P. L. (2013). A call to arms: on refining Plasmodium vivax microsatellite marker panels for comparing global diversity. Malaria Journal 12, 447. doi: 10.1186/1475-2875-12-447.CrossRefGoogle Scholar
Taylor, J. E., Pacheco, M. A., Bacon, D. J., Beg, M. A., Machado, R. L. D., Fairhurst, R. M., Herrera, S., Kim, J. Y., Menard, D., Póvoa, M. M., Villegas, L. M., Snounou, G., Cui, L., Zeyrek, F. Y. and Escalante, A. A. (2013). The evolutionary history of Plasmodium vivax as inferred from mitochondrial genomes: parasite genetic diversity in the Americas. Molecular Biology and Evolution 30, 20502064. doi: 10.1093/molbev/mst104.CrossRefGoogle ScholarPubMed
Tibayrenc, M. and Ayala, F. J. (2014). New insights into clonality and panmixia in Plasmodium and Toxoplasma . Advances in Parasitology 84, 253268. doi: 10.1016/B978-0-12-800099-1.00005-3.CrossRefGoogle ScholarPubMed
Van den Eede, P., Erhart, A., van der Auwera, G., van Overmeir, C., Thang, N. D., Hung le, X., Anné, J. and D'Alessandro, U. (2010 a). High complexity of Plasmodium vivax infections in symptomatic patients from a rural community in central Vietnam detected by microsatellite genotyping. American Journal of Tropical Medicine and Hygiene 82, 223227. doi: 10.4269/ajtmh.2010.09-0458.CrossRefGoogle ScholarPubMed
Van den Eede, P., van der Auwera, G., Delgado, C., Huyse, T., Soto-Calle, V. E., Gamboa, D., Grande, T., Rodríguez, H., Llanos, A., Anné, J., Erhart, A. and D'Alessandro, U. (2010 b). Multilocus genotyping reveals high heterogeneity and strong local population structure of the Plasmodium vivax population in the Peruvian Amazon. Malaria Journal 9, 151. doi: 10.1186/1475-2875-9-151.CrossRefGoogle ScholarPubMed
Vittor, A. Y., Gilman, R. H., Tielsch, J., Glass, G., Shields, T., Lozano, W. S., Pinedo-Cancino, V. and Patz, J. A. (2006). The effect of deforestation on the human-biting rate of Anopheles darlingi, the primary vector of falciparum malaria in the Peruvian Amazon. American Journal of Tropical Medicine and Hygiene 7, 311.CrossRefGoogle Scholar
Vittor, A. Y., Pan, W., Gilman, R. H., Tielsch, J., Glass, G., Shields, T., Sanchez-Lozano, W., Pinedo, V. V., Salas-Cobos, E., Flores, S. and Patz, J. A. (2009). Linking deforestation to malaria in the Amazon: characterization of the breeding habitat of the principal malaria vector, Anopheles darlingi . American Journal of Tropical Medicine and Hygiene 81, 512.Google ScholarPubMed
World Health Organization (2013). World Malaria Report 2013. World Health Organization, Geneva, p. 284. http://who.int/malaria/publications/world_malaria_report_2013/report/en/ Google Scholar
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