Skip to main content
Top
Published in: Malaria Journal 1/2015

Open Access 01-12-2015 | Research

Longitudinal analysis of Plasmodium falciparum genetic variation in Turbo, Colombia: implications for malaria control and elimination

Authors: Stella M. Chenet, Jesse E. Taylor, Silvia Blair, Lina Zuluaga, Ananias A. Escalante

Published in: Malaria Journal | Issue 1/2015

Login to get access

Abstract

Background

Malaria programmes estimate changes in prevalence to evaluate their efficacy. In this study, parasite genetic data was used to explore how the demography of the parasite population can inform about the processes driving variation in prevalence. In particular, how changes in treatment and population movement have affected malaria prevalence in an area with seasonal malaria.

Methods

Samples of Plasmodium falciparum collected over 8 years from a population in Turbo, Colombia were genotyped at nine microsatellite loci and three drug-resistance loci. These data were analysed using several population genetic methods to detect changes in parasite genetic diversity and population structure. In addition, a coalescent-based method was used to estimate substitution rates at the microsatellite loci.

Results

The estimated mean microsatellite substitution rates varied between 5.35 × 10−3 and 3.77 × 10−2 substitutions/locus/month. Cluster analysis identified six distinct parasite clusters, five of which persisted for the full duration of the study. However, the frequencies of the clusters varied significantly between years, consistent with a small effective population size.

Conclusions

Malaria control programmes can detect re-introductions and changes in transmission using rapidly evolving microsatellite loci. In this population, the steadily decreasing diversity and the relatively constant effective population size suggest that an increase in malaria prevalence from 2004 to 2007 was primarily driven by local rather than imported cases.
Appendix
Available only for authorised users
Literature
1.
go back to reference Arevalo-Herrera M, Quiñones ML, Guerra C, Céspedes N, Giron S, Ahumada M, et al. Malaria in selected non-Amazonian countries of Latin America. Acta Trop. 2012;121:303–14.PubMedCentralCrossRefPubMed Arevalo-Herrera M, Quiñones ML, Guerra C, Céspedes N, Giron S, Ahumada M, et al. Malaria in selected non-Amazonian countries of Latin America. Acta Trop. 2012;121:303–14.PubMedCentralCrossRefPubMed
3.
go back to reference Taylor JE, Pacheco MA, Bacon DJ, Beg MA, Machado RL, Fairhurst RM, et al. The evolutionary history of Plasmodium vivax as inferred from mitochondrial genomes: parasite genetic diversity in the Americas. Mol Biol Evol. 2013;30:2050–64.PubMedCentralCrossRefPubMed Taylor JE, Pacheco MA, Bacon DJ, Beg MA, Machado RL, Fairhurst RM, et al. The evolutionary history of Plasmodium vivax as inferred from mitochondrial genomes: parasite genetic diversity in the Americas. Mol Biol Evol. 2013;30:2050–64.PubMedCentralCrossRefPubMed
4.
go back to reference McCollum AM, Mueller K, Villegas L, Udhayakumar V, Escalante AA. Common origin and fixation of Plasmodium falciparum dhfr and dhps mutations associated with sulfadoxine–pyrimethamine resistance in a low-transmission area in South America. Antimicrob Agents Chemother. 2007;51:2085–91.PubMedCentralCrossRefPubMed McCollum AM, Mueller K, Villegas L, Udhayakumar V, Escalante AA. Common origin and fixation of Plasmodium falciparum dhfr and dhps mutations associated with sulfadoxine–pyrimethamine resistance in a low-transmission area in South America. Antimicrob Agents Chemother. 2007;51:2085–91.PubMedCentralCrossRefPubMed
5.
go back to reference Corredor V, Murillo C, Echeverry DF, Benavides J, Pearce RJ, Roper C, et al. Origin and dissemination across the Colombian Andes mountain range of sulfadoxine–pyrimethamine resistance in Plasmodium falciparum. Antimicrob Agents Chemother. 2010;54:3121–5.PubMedCentralCrossRefPubMed Corredor V, Murillo C, Echeverry DF, Benavides J, Pearce RJ, Roper C, et al. Origin and dissemination across the Colombian Andes mountain range of sulfadoxine–pyrimethamine resistance in Plasmodium falciparum. Antimicrob Agents Chemother. 2010;54:3121–5.PubMedCentralCrossRefPubMed
6.
go back to reference Griffing SM, Viana GM, Mixson-Hayden T, Sridaran S, Alam MT, de Oliveira AM, et al. Historical shifts in Brazilian P. falciparum population structure and drug resistance alleles. PLoS One. 2013;8:e58984.PubMedCentralCrossRefPubMed Griffing SM, Viana GM, Mixson-Hayden T, Sridaran S, Alam MT, de Oliveira AM, et al. Historical shifts in Brazilian P. falciparum population structure and drug resistance alleles. PLoS One. 2013;8:e58984.PubMedCentralCrossRefPubMed
7.
go back to reference Echeverry DF, Nair S, Osorio L, Menon S, Murillo C, Anderson TJ. Long term persistence of clonal malaria parasite Plasmodium falciparum lineages in the Colombian Pacific region. BMC Genet. 2013;14:2.PubMedCentralCrossRefPubMed Echeverry DF, Nair S, Osorio L, Menon S, Murillo C, Anderson TJ. Long term persistence of clonal malaria parasite Plasmodium falciparum lineages in the Colombian Pacific region. BMC Genet. 2013;14:2.PubMedCentralCrossRefPubMed
8.
go back to reference Mueller I, Schoepflin S, Smith TA, Benton KL, Bretscher MT, Lin E, et al. Force of infection is key to understanding the epidemiology of Plasmodium falciparum malaria in Papua New Guinean children. Proc Natl Acad Sci USA. 2012;109:10030–5.PubMedCentralCrossRefPubMed Mueller I, Schoepflin S, Smith TA, Benton KL, Bretscher MT, Lin E, et al. Force of infection is key to understanding the epidemiology of Plasmodium falciparum malaria in Papua New Guinean children. Proc Natl Acad Sci USA. 2012;109:10030–5.PubMedCentralCrossRefPubMed
9.
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.PubMedCentralCrossRefPubMed 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.PubMedCentralCrossRefPubMed
10.
go back to reference Escalante AA, Ferreira MU, Vinetz JM, Volkman SK, Cui L, Gamboa D, et al. Malaria molecular epidemiology: lessons from the international centers of excellence for malaria research network. Am J Trop Med Hyg. 2015; pii: 15-0005 [Epub ahead of print]. Escalante AA, Ferreira MU, Vinetz JM, Volkman SK, Cui L, Gamboa D, et al. Malaria molecular epidemiology: lessons from the international centers of excellence for malaria research network. Am J Trop Med Hyg. 2015; pii: 15-0005 [Epub ahead of print].
11.
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;22:7067–72.CrossRef 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;22:7067–72.CrossRef
12.
go back to reference Daniels R, Chang HH, 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;4:e60780.CrossRef Daniels R, Chang HH, 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;4:e60780.CrossRef
13.
go back to reference Rodriguez JC, Uribe GA, Araujo RM, Narvaez PC, Valencia SH. Epidemiology and control of malaria in Colombia. Mem Inst Oswaldo Cruz. 2011;106:114–22.CrossRefPubMed Rodriguez JC, Uribe GA, Araujo RM, Narvaez PC, Valencia SH. Epidemiology and control of malaria in Colombia. Mem Inst Oswaldo Cruz. 2011;106:114–22.CrossRefPubMed
14.
go back to reference Blair S, Carmona-Fonseca J, Piñeros JG, Ríos A, Alvarez T, Alvarez G, et al. Therapeutic efficacy test in malaria falciparum in Antioquia, Colombia. Malar J. 2006;5:14.PubMedCentralCrossRefPubMed Blair S, Carmona-Fonseca J, Piñeros JG, Ríos A, Alvarez T, Alvarez G, et al. Therapeutic efficacy test in malaria falciparum in Antioquia, Colombia. Malar J. 2006;5:14.PubMedCentralCrossRefPubMed
15.
go back to reference Rambaut A, Pybus OG, Nelson M, Viboud C, Taubenberger J, Holmes E. The genomic and epidemiological dynamics of human influenza A virus. Nature. 2008;453:615–9.PubMedCentralCrossRefPubMed Rambaut A, Pybus OG, Nelson M, Viboud C, Taubenberger J, Holmes E. The genomic and epidemiological dynamics of human influenza A virus. Nature. 2008;453:615–9.PubMedCentralCrossRefPubMed
16.
go back to reference Carrington C, Foster J, Pybus O, Bennett S, Holmes E. Invasion and maintenance of dengue virus type 2 and type 4 in the Americas. J Virol. 2005;79:14680–7.PubMedCentralCrossRefPubMed Carrington C, Foster J, Pybus O, Bennett S, Holmes E. Invasion and maintenance of dengue virus type 2 and type 4 in the Americas. J Virol. 2005;79:14680–7.PubMedCentralCrossRefPubMed
17.
go back to reference Bennett SN, Drummond AJ, Kapan DD, Suchard MA, Muñoz-Jordán JL, Pybus OG, et al. Epidemic dynamics revealed in dengue evolution. Mol Biol Evol. 2010;27:811–8.PubMedCentralCrossRefPubMed Bennett SN, Drummond AJ, Kapan DD, Suchard MA, Muñoz-Jordán JL, Pybus OG, et al. Epidemic dynamics revealed in dengue evolution. Mol Biol Evol. 2010;27:811–8.PubMedCentralCrossRefPubMed
18.
go back to reference Alvarez G, Tobón A, Piñeros JG, Ríos A, Blair S. Dynamics of Plasmodium falciparum parasitemia regarding combined treatment regimens for acute uncomplicated malaria, Antioquia, Colombia. Am J Trop Med Hyg. 2010;83:90–6.PubMedCentralCrossRefPubMed Alvarez G, Tobón A, Piñeros JG, Ríos A, Blair S. Dynamics of Plasmodium falciparum parasitemia regarding combined treatment regimens for acute uncomplicated malaria, Antioquia, Colombia. Am J Trop Med Hyg. 2010;83:90–6.PubMedCentralCrossRefPubMed
19.
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;119:113–25.CrossRefPubMed 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;119:113–25.CrossRefPubMed
20.
go back to reference Griffing S, Syphard L, Sridaran S, McCollum AM, Mixson-Hayden T, Vinayak S, et al. pfmdr1 amplification and fixation of pfcrt chloroquine resistance alleles in Plasmodium falciparum in Venezuela. Antimicrob Agents Chemother. 2010;54:1572–9.PubMedCentralCrossRefPubMed Griffing S, Syphard L, Sridaran S, McCollum AM, Mixson-Hayden T, Vinayak S, et al. pfmdr1 amplification and fixation of pfcrt chloroquine resistance alleles in Plasmodium falciparum in Venezuela. Antimicrob Agents Chemother. 2010;54:1572–9.PubMedCentralCrossRefPubMed
21.
go back to reference Vinayak S, Alam MT, Mixson-Hayden T, McCollum AM, Sem R, Shah NK, et al. Origin and evolution of sulfadoxine resistant Plasmodium falciparum. PLoS Pathog. 2010;6:e1000830.PubMedCentralCrossRefPubMed Vinayak S, Alam MT, Mixson-Hayden T, McCollum AM, Sem R, Shah NK, et al. Origin and evolution of sulfadoxine resistant Plasmodium falciparum. PLoS Pathog. 2010;6:e1000830.PubMedCentralCrossRefPubMed
22.
go back to reference McCollum AM, Schneider KA, Griffing SM, Zhou Z, Kariuki S, Ter-Kuile F, et al. Differences in selective pressure on dhps and dhfr drug resistant mutations in western Kenya. Malar J. 2012;11:77.PubMedCentralCrossRefPubMed McCollum AM, Schneider KA, Griffing SM, Zhou Z, Kariuki S, Ter-Kuile F, et al. Differences in selective pressure on dhps and dhfr drug resistant mutations in western Kenya. Malar J. 2012;11:77.PubMedCentralCrossRefPubMed
23.
go back to reference Nash D, Nair S, Mayxay M, Newton PN, Guthmann JP, Nosten F, et al. Selection strength and hitchhiking around two anti-malarial resistance genes. Proc Biol Sci. 2005;272:1153–61.PubMedCentralCrossRefPubMed Nash D, Nair S, Mayxay M, Newton PN, Guthmann JP, Nosten F, et al. Selection strength and hitchhiking around two anti-malarial resistance genes. Proc Biol Sci. 2005;272:1153–61.PubMedCentralCrossRefPubMed
24.
go back to reference Pritchard JK, Stephens M, Donnelly P. Inference of population structure using multilocus genotype data. Genetics. 2000;155:945–59.PubMedCentralPubMed Pritchard JK, Stephens M, Donnelly P. Inference of population structure using multilocus genotype data. Genetics. 2000;155:945–59.PubMedCentralPubMed
25.
go back to reference Bandelt H-J, Forster P, Röhl A. Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol. 1999;16:37–48.CrossRefPubMed Bandelt H-J, Forster P, Röhl A. Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol. 1999;16:37–48.CrossRefPubMed
26.
go back to reference Haubold B, Hudson RR. LIAN, 3.0: detecting linkage disequilibrium in multilocus data. Linkage Analysis. Bioinformatics. 2000;16:847–8.CrossRefPubMed Haubold B, Hudson RR. LIAN, 3.0: detecting linkage disequilibrium in multilocus data. Linkage Analysis. Bioinformatics. 2000;16:847–8.CrossRefPubMed
27.
go back to reference Excoffier L, Lischer HE. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour. 2010;10:564–7.CrossRefPubMed Excoffier L, Lischer HE. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour. 2010;10:564–7.CrossRefPubMed
28.
29.
go back to reference Wu CH, Drummond AJ. Joint inference of microsatellite mutation models, population history and genealogies using transdimensional Markov Chain Monte Carlo. Genetics. 2011;188:151–64.PubMedCentralCrossRefPubMed Wu CH, Drummond AJ. Joint inference of microsatellite mutation models, population history and genealogies using transdimensional Markov Chain Monte Carlo. Genetics. 2011;188:151–64.PubMedCentralCrossRefPubMed
30.
go back to reference Sainudiin R, Durrett RT, Aquadro CF, Nielsen R. Microsatellite mutation models: insights from a comparison of humans and chimpanzees. Genetics. 2004;168:383–95.PubMedCentralCrossRefPubMed Sainudiin R, Durrett RT, Aquadro CF, Nielsen R. Microsatellite mutation models: insights from a comparison of humans and chimpanzees. Genetics. 2004;168:383–95.PubMedCentralCrossRefPubMed
32.
go back to reference Agudelo OM, Aristizabal BH, Yanow SK, Arango E, Carmona-Fonseca J, Maestre A. Submicroscopic infection of placenta by Plasmodium produces Th1/Th2 cytokine imbalance, inflammation and hypoxia in women from north-west Colombia. Malar J. 2014;13:122.PubMedCentralCrossRefPubMed Agudelo OM, Aristizabal BH, Yanow SK, Arango E, Carmona-Fonseca J, Maestre A. Submicroscopic infection of placenta by Plasmodium produces Th1/Th2 cytokine imbalance, inflammation and hypoxia in women from north-west Colombia. Malar J. 2014;13:122.PubMedCentralCrossRefPubMed
35.
go back to reference Su X, Ferdig MT, Huang Y, Huynh CQ, Liu A, You J, et al. A genetic map and recombination parameters of the human malaria parasite Plasmodium falciparum. Science. 1999;286:1351–3.CrossRefPubMed Su X, Ferdig MT, Huang Y, Huynh CQ, Liu A, You J, et al. A genetic map and recombination parameters of the human malaria parasite Plasmodium falciparum. Science. 1999;286:1351–3.CrossRefPubMed
36.
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.PubMedCentralCrossRefPubMed Chenet SM, Schneider KA, Villegas L, Escalante AA. Local population structure of Plasmodium: impact on malaria control and elimination. Malar J. 2012;11:412.PubMedCentralCrossRefPubMed
37.
go back to reference Kublin JG, Cortese JF, Njunju EM, Mukadam RA, Wirima JJ, Kazembe PN, et al. Reemergence of chloroquine-sensitive Plasmodium falciparum malaria after cessation of chloroquine use in Malawi. J Infect Dis. 2003;187:1870–5.CrossRefPubMed Kublin JG, Cortese JF, Njunju EM, Mukadam RA, Wirima JJ, Kazembe PN, et al. Reemergence of chloroquine-sensitive Plasmodium falciparum malaria after cessation of chloroquine use in Malawi. J Infect Dis. 2003;187:1870–5.CrossRefPubMed
38.
go back to reference Zhou Z, Griffing SM, de Oliveira AM, McCollum AM, Quezada WM, Arrospide N, et al. Decline in sulfadoxine-pyrimethamine-resistant alleles after change in drug policy in the Amazon region of Peru. Antimicrob Agents Chemother. 2008;52:739–41.PubMedCentralCrossRefPubMed Zhou Z, Griffing SM, de Oliveira AM, McCollum AM, Quezada WM, Arrospide N, et al. Decline in sulfadoxine-pyrimethamine-resistant alleles after change in drug policy in the Amazon region of Peru. Antimicrob Agents Chemother. 2008;52:739–41.PubMedCentralCrossRefPubMed
Metadata
Title
Longitudinal analysis of Plasmodium falciparum genetic variation in Turbo, Colombia: implications for malaria control and elimination
Authors
Stella M. Chenet
Jesse E. Taylor
Silvia Blair
Lina Zuluaga
Ananias A. Escalante
Publication date
01-12-2015
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2015
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-015-0887-9

Other articles of this Issue 1/2015

Malaria Journal 1/2015 Go to the issue