Skip to main content
Top
Published in: Malaria Journal 1/2019

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

High Plasmodium falciparum genetic diversity and temporal stability despite control efforts in high transmission settings along the international border between Zambia and the Democratic Republic of the Congo

Authors: Julia C. Pringle, Amy Wesolowski, Sophie Berube, Tamaki Kobayashi, Mary E. Gebhardt, Modest Mulenga, Mike Chaponda, Thierry Bobanga, Jonathan J. Juliano, Steven Meshnick, William J. Moss, Giovanna Carpi, Douglas E. Norris

Published in: Malaria Journal | Issue 1/2019

Login to get access

Abstract

Background

While the utility of parasite genotyping for malaria elimination has been extensively documented in low to moderate transmission settings, it has been less well-characterized in holoendemic regions. High malaria burden settings have received renewed attention acknowledging their critical role in malaria elimination. Defining the role for parasite genomics in driving these high burden settings towards elimination will enhance future control programme planning.

Methods

Amplicon deep sequencing was used to characterize parasite population genetic diversity at polymorphic Plasmodium falciparum loci, Pfama1 and Pfcsp, at two timepoints in June–July 2016 and January–March 2017 in a high transmission region along the international border between Luapula Province, Zambia and Haut-Katanga Province, the Democratic Republic of the Congo (DRC).

Results

High genetic diversity was observed across both seasons and in both countries. No evidence of population structure was observed between parasite populations on either side of the border, suggesting that this region may be one contiguous transmission zone. Despite a decline in parasite prevalence at the sampling locations in Haut-Katanga Province, no genetic signatures of a population bottleneck were detected, suggesting that larger declines in transmission may be required to reduce parasite genetic diversity. Analysing rare variants may be a suitable alternative approach for detecting epidemiologically important genetic signatures in highly diverse populations; however, the challenge is distinguishing true signals from potential artifacts introduced by small sample sizes.

Conclusions

Continuing to explore and document the utility of various parasite genotyping approaches for understanding malaria transmission in holoendemic settings will be valuable to future control and elimination programmes, empowering evidence-based selection of tools and methods to address pertinent questions, thus enabling more efficient resource allocation.
Appendix
Available only for authorised users
Literature
1.
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;526:207–11.PubMedPubMedCentralCrossRef 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;526:207–11.PubMedPubMedCentralCrossRef
2.
go back to reference Cibulskis RE, Alonso P, Aponte J, Aregawi M, Barrette A, Bergeron L, et al. Malaria: global progress 2000–2015 and future challenges. Infect Dis Poverty. 2016;5:61.PubMedPubMedCentralCrossRef Cibulskis RE, Alonso P, Aponte J, Aregawi M, Barrette A, Bergeron L, et al. Malaria: global progress 2000–2015 and future challenges. Infect Dis Poverty. 2016;5:61.PubMedPubMedCentralCrossRef
3.
go back to reference Newby G, Bennett A, Larson E, Cotter C, Shretta R, Phillips AA, et al. The path to eradication: a progress report on the malaria-eliminating countries. Lancet. 2016;387:1775–84.PubMedCrossRef Newby G, Bennett A, Larson E, Cotter C, Shretta R, Phillips AA, et al. The path to eradication: a progress report on the malaria-eliminating countries. Lancet. 2016;387:1775–84.PubMedCrossRef
4.
go back to reference Mukonka VM, Chanda E, Haque U, Kamuliwo M, Mushinge G, Chileshe J, et al. High burden of malaria following scale-up of control interventions in Nchelenge District, Luapula Province, Zambia. Malar J. 2014;13:153.PubMedPubMedCentralCrossRef Mukonka VM, Chanda E, Haque U, Kamuliwo M, Mushinge G, Chileshe J, et al. High burden of malaria following scale-up of control interventions in Nchelenge District, Luapula Province, Zambia. Malar J. 2014;13:153.PubMedPubMedCentralCrossRef
5.
go back to reference WHO. World malaria report 2018. Geneva: World Health Organization; 2018. WHO. World malaria report 2018. Geneva: World Health Organization; 2018.
6.
go back to reference World Health Organization & Roll Back Malaria Partnership to End Malaria. High burden to high impact: a targeted malaria response. Geneva: World Health Organization; 2018. World Health Organization & Roll Back Malaria Partnership to End Malaria. High burden to high impact: a targeted malaria response. Geneva: World Health Organization; 2018.
7.
go back to reference Auburn S, Barry AE. Dissecting malaria biology and epidemiology using population genetics and genomics. Int J Parasitol. 2017;47:77–85.PubMedCrossRef Auburn S, Barry AE. Dissecting malaria biology and epidemiology using population genetics and genomics. Int J Parasitol. 2017;47:77–85.PubMedCrossRef
9.
go back to reference Le Roch KG, Chung DWD, Ponts N. Genomics and integrated systems biology in Plasmodium falciparum: a path to malaria control and eradication. Parasite Immunol. 2012;34:50–60.PubMedPubMedCentralCrossRef Le Roch KG, Chung DWD, Ponts N. Genomics and integrated systems biology in Plasmodium falciparum: a path to malaria control and eradication. Parasite Immunol. 2012;34:50–60.PubMedPubMedCentralCrossRef
10.
go back to reference Pringle JC, Tessema S, Wesolowski A, Chen A, Murphy M, Carpi G, et al. Genetic evidence of focal Plasmodium falciparum transmission in a pre-elimination setting in Southern Province, Zambia. J Infect Dis. 2019;219:1254–63.PubMedCrossRef Pringle JC, Tessema S, Wesolowski A, Chen A, Murphy M, Carpi G, et al. Genetic evidence of focal Plasmodium falciparum transmission in a pre-elimination setting in Southern Province, Zambia. J Infect Dis. 2019;219:1254–63.PubMedCrossRef
11.
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;8:e60780.PubMedPubMedCentralCrossRef 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;8:e60780.PubMedPubMedCentralCrossRef
12.
go back to reference Daniels RF, Schaffner SF, Wenger EA, Proctor JL, Chang H-H, Wong W, et al. Modeling malaria genomics reveals transmission decline and rebound in Senegal. Proc Natl Acad Sci USA. 2015;112:7067–72.PubMedCrossRefPubMedCentral Daniels RF, Schaffner SF, Wenger EA, Proctor JL, Chang H-H, Wong W, et al. Modeling malaria genomics reveals transmission decline and rebound in Senegal. Proc Natl Acad Sci USA. 2015;112:7067–72.PubMedCrossRefPubMedCentral
13.
go back to reference Ofosu-Okyere A, Mackinnon MJ, Sowa MP, Koram KA, Nkrumah F, Osei YD, et al. Novel Plasmodium falciparum clones and rising clone multiplicities are associated with the increase in malaria morbidity in Ghanaian children during the transition into the high transmission season. Parasitology. 2001;123:113–23.PubMedCrossRef Ofosu-Okyere A, Mackinnon MJ, Sowa MP, Koram KA, Nkrumah F, Osei YD, et al. Novel Plasmodium falciparum clones and rising clone multiplicities are associated with the increase in malaria morbidity in Ghanaian children during the transition into the high transmission season. Parasitology. 2001;123:113–23.PubMedCrossRef
14.
go back to reference Gatei W, Kariuki S, Hawley W, ter Kuile F, Terlouw D, Phillips-Howard P, et al. Effects of transmission reduction by insecticide-treated bed nets (ITNs) on parasite genetics population structure: I. The genetic diversity of Plasmodium falciparum parasites by microsatellite markers in western Kenya. Malar J. 2010;9:353.PubMedPubMedCentralCrossRef Gatei W, Kariuki S, Hawley W, ter Kuile F, Terlouw D, Phillips-Howard P, et al. Effects of transmission reduction by insecticide-treated bed nets (ITNs) on parasite genetics population structure: I. The genetic diversity of Plasmodium falciparum parasites by microsatellite markers in western Kenya. Malar J. 2010;9:353.PubMedPubMedCentralCrossRef
15.
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;93:79–86.PubMedPubMedCentralCrossRef 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;93:79–86.PubMedPubMedCentralCrossRef
16.
go back to reference Baliraine FN, Afrane YA, Amenya DA, Bonizzoni M, Vardo-Zalik AM, Menge DM, et al. A cohort study of Plasmodium falciparum infection dynamics in Western Kenya Highlands. BMC Infect Dis. 2010;10:283.PubMedPubMedCentralCrossRef Baliraine FN, Afrane YA, Amenya DA, Bonizzoni M, Vardo-Zalik AM, Menge DM, et al. A cohort study of Plasmodium falciparum infection dynamics in Western Kenya Highlands. BMC Infect Dis. 2010;10:283.PubMedPubMedCentralCrossRef
17.
go back to reference Ibara-Okabande R, Koukouikila-Koussounda F, Ndounga M, Vouvoungui J, Malonga V, Casimiro PN, et al. Reduction of multiplicity of infections but no change in msp2 genetic diversity in Plasmodium falciparum isolates from Congolese children after introduction of artemisinin-combination therapy. Malar J. 2012;11:410.PubMedPubMedCentralCrossRef Ibara-Okabande R, Koukouikila-Koussounda F, Ndounga M, Vouvoungui J, Malonga V, Casimiro PN, et al. Reduction of multiplicity of infections but no change in msp2 genetic diversity in Plasmodium falciparum isolates from Congolese children after introduction of artemisinin-combination therapy. Malar J. 2012;11:410.PubMedPubMedCentralCrossRef
18.
go back to reference Beck HP, Felger I, Huber W, Steiger S, Smith T, Weiss N, et al. Analysis of multiple Plasmodium falciparum infections in Tanzanian children during the phase III trial of the malaria vaccine SPf66. J Infect Dis. 1997;175:921–6.PubMedCrossRef Beck HP, Felger I, Huber W, Steiger S, Smith T, Weiss N, et al. Analysis of multiple Plasmodium falciparum infections in Tanzanian children during the phase III trial of the malaria vaccine SPf66. J Infect Dis. 1997;175:921–6.PubMedCrossRef
19.
go back to reference Buchholz U, Kobbe R, Danquah I, Zanger P, Reither K, Abruquah HH, et al. Multiplicity of Plasmodium falciparum infection following intermittent preventive treatment in infants. Malar J. 2010;9:244.PubMedPubMedCentralCrossRef Buchholz U, Kobbe R, Danquah I, Zanger P, Reither K, Abruquah HH, et al. Multiplicity of Plasmodium falciparum infection following intermittent preventive treatment in infants. Malar J. 2010;9:244.PubMedPubMedCentralCrossRef
20.
go back to reference Lo E, Lam N, Hemming-Schroeder E, Nguyen J, Zhou G, Lee M-C, et al. Frequent spread of Plasmodium vivax malaria maintains high genetic diversity at the Myanmar-China border, without distance and landscape barriers. J Infect Dis. 2017;216:1254–63.PubMedPubMedCentralCrossRef Lo E, Lam N, Hemming-Schroeder E, Nguyen J, Zhou G, Lee M-C, et al. Frequent spread of Plasmodium vivax malaria maintains high genetic diversity at the Myanmar-China border, without distance and landscape barriers. J Infect Dis. 2017;216:1254–63.PubMedPubMedCentralCrossRef
21.
go back to reference Al-Hamidhi S, Mahdy MAK, Idris MA, Bin Dajem SM, Al-Sheikh AAH, Al-Qahtani A, et al. The prospect of malaria elimination in the Arabian Peninsula: a population genetic approach. Infect Genet Evol. 2014;27:25–31.PubMedCrossRef Al-Hamidhi S, Mahdy MAK, Idris MA, Bin Dajem SM, Al-Sheikh AAH, Al-Qahtani A, et al. The prospect of malaria elimination in the Arabian Peninsula: a population genetic approach. Infect Genet Evol. 2014;27:25–31.PubMedCrossRef
22.
go back to reference Tessema S, Wesolowski A, Chen A, Murphy M, Wilheim J, Mupiri A-R, et al. Using parasite genetic and human mobility data to infer local and cross-border malaria connectivity in Southern Africa. Elife. 2019;8:e43510.PubMedPubMedCentralCrossRef Tessema S, Wesolowski A, Chen A, Murphy M, Wilheim J, Mupiri A-R, et al. Using parasite genetic and human mobility data to infer local and cross-border malaria connectivity in Southern Africa. Elife. 2019;8:e43510.PubMedPubMedCentralCrossRef
23.
go back to reference Lo E, Zhou G, Oo W, Lee M-C, 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 M-C, 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
24.
go back to reference Republic of Zambia Ministry of Health. Zambia malaria indicator survey 2018. Lusaka: Republic of Zambia Ministry of Health; 2018. Republic of Zambia Ministry of Health. Zambia malaria indicator survey 2018. Lusaka: Republic of Zambia Ministry of Health; 2018.
26.
go back to reference Moss WJ, Dorsey G, Mueller I, Laufer MK, Krogstad DJ, Vinetz JM, et al. Malaria epidemiology and control within the International Centers of Excellence for Malaria Research. Am J Trop Med Hyg. 2015;93:5–15.PubMedPubMedCentralCrossRef Moss WJ, Dorsey G, Mueller I, Laufer MK, Krogstad DJ, Vinetz JM, et al. Malaria epidemiology and control within the International Centers of Excellence for Malaria Research. Am J Trop Med Hyg. 2015;93:5–15.PubMedPubMedCentralCrossRef
27.
go back to reference Banque Mondiale. République Démocratique du Congo Deuxième Enquête Démographique et de Santé (EDS-RDC II 2013–2014). Le Fonds mondial de lutte contre le SIDA, la tuberculose et le paludisme. Septembre 2014. Banque Mondiale. République Démocratique du Congo Deuxième Enquête Démographique et de Santé (EDS-RDC II 2013–2014). Le Fonds mondial de lutte contre le SIDA, la tuberculose et le paludisme. Septembre 2014.
28.
go back to reference Parr JB, Belson C, Patel JC, Hoffman IF, Kamthunzi P, Martinson F, et al. Estimation of Plasmodium falciparum transmission intensity in Lilongwe, Malawi, by microscopy, rapid diagnostic testing, and nucleic acid detection. Am J Trop Med Hyg. 2016;95:373–7.PubMedPubMedCentralCrossRef Parr JB, Belson C, Patel JC, Hoffman IF, Kamthunzi P, Martinson F, et al. Estimation of Plasmodium falciparum transmission intensity in Lilongwe, Malawi, by microscopy, rapid diagnostic testing, and nucleic acid detection. Am J Trop Med Hyg. 2016;95:373–7.PubMedPubMedCentralCrossRef
29.
go back to reference Pringle JC, Carpi G, Almagro-Garcia J, Zhu SJ, Kobayashi T, Mulenga M, et al. RTS, S/AS01 malaria vaccine mismatch observed among Plasmodium falciparum isolates from southern and central Africa and globally. Sci Rep. 2018;8:6622.PubMedPubMedCentralCrossRef Pringle JC, Carpi G, Almagro-Garcia J, Zhu SJ, Kobayashi T, Mulenga M, et al. RTS, S/AS01 malaria vaccine mismatch observed among Plasmodium falciparum isolates from southern and central Africa and globally. Sci Rep. 2018;8:6622.PubMedPubMedCentralCrossRef
30.
go back to reference Illumina. 16S Metagenomic sequencing library preparation. 2013;(B):1–28. Illumina. 16S Metagenomic sequencing library preparation. 2013;(B):1–28.
31.
go back to reference Hathaway NJ, Parobek CM, Juliano JJ, Bailey JA. SeekDeep: single-base resolution de novo clustering for amplicon deep sequencing. Nucleic Acids Res. 2018;46:e21.PubMedCrossRef Hathaway NJ, Parobek CM, Juliano JJ, Bailey JA. SeekDeep: single-base resolution de novo clustering for amplicon deep sequencing. Nucleic Acids Res. 2018;46:e21.PubMedCrossRef
32.
go back to reference ESRI. ArcGIS Desktop: release 10.6. Redlands: Environmental Systems Research Institute; 2018. ESRI. ArcGIS Desktop: release 10.6. Redlands: Environmental Systems Research Institute; 2018.
34.
go back to reference Jombart T. adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics. 2008;24:1403–5.PubMedCrossRef Jombart T. adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics. 2008;24:1403–5.PubMedCrossRef
35.
go back to reference Jombart T, Devillard S, Balloux F. Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet. 2010;11:94.PubMedPubMedCentralCrossRef Jombart T, Devillard S, Balloux F. Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet. 2010;11:94.PubMedPubMedCentralCrossRef
36.
go back to reference Clement M, Posada D, Crandall KA. TCS: a computer program to estimate gene genealogies. Mol Ecol. 2000;9:1657–9.PubMedCrossRef Clement M, Posada D, Crandall KA. TCS: a computer program to estimate gene genealogies. Mol Ecol. 2000;9:1657–9.PubMedCrossRef
37.
go back to reference Múrias dos Santos A, Cabezas MP, Tavares AI, Xavier R, Branco M. tcsBU: a tool to extend TCS network layout and visualization. Bioinformatics. 2016;32:627–8.PubMedCrossRef Múrias dos Santos A, Cabezas MP, Tavares AI, Xavier R, Branco M. tcsBU: a tool to extend TCS network layout and visualization. Bioinformatics. 2016;32:627–8.PubMedCrossRef
38.
go back to reference Luikart G, Allendorf FW, Cornuet JM, Sherwin WB. Distortion of allele frequency distributions provides a test for recent population bottlenecks. J Hered. 1998;89:238–47.PubMedCrossRef Luikart G, Allendorf FW, Cornuet JM, Sherwin WB. Distortion of allele frequency distributions provides a test for recent population bottlenecks. J Hered. 1998;89:238–47.PubMedCrossRef
39.
go back to reference Gravel S, Henn BM, Gutenkunst RN, Indap AR, Marth GT, Clark AG, et al. Demographic history and rare allele sharing among human populations. Proc Natl Acad Sci USA. 2011;108:11983–8.PubMedCrossRefPubMedCentral Gravel S, Henn BM, Gutenkunst RN, Indap AR, Marth GT, Clark AG, et al. Demographic history and rare allele sharing among human populations. Proc Natl Acad Sci USA. 2011;108:11983–8.PubMedCrossRefPubMedCentral
40.
go back to reference O’Connor TD, Fu W, Mychaleckyj JC, Logsdon B, Auer P, Carlson CS, et al. Rare variation facilitates inferences of fine-scale population structure in humans. Mol Biol Evol. 2015;32:653–60.PubMedCrossRef O’Connor TD, Fu W, Mychaleckyj JC, Logsdon B, Auer P, Carlson CS, et al. Rare variation facilitates inferences of fine-scale population structure in humans. Mol Biol Evol. 2015;32:653–60.PubMedCrossRef
41.
go back to reference Goudet J. hierfstat, a package for r to compute and test hierarchical F-statistics. Mol Ecol Notes. 2005;5:184–6.CrossRef Goudet J. hierfstat, a package for r to compute and test hierarchical F-statistics. Mol Ecol Notes. 2005;5:184–6.CrossRef
42.
go back to reference Aydemir O, Janko M, Hathaway NJ, Verity R, Mwandagalirwa MK, Tshefu AK, et al. Drug-resistance and population structure of Plasmodium falciparum across the Democratic Republic of Congo using high-throughput molecular inversion probes. J Infect Dis. 2018;218:946–55.PubMedPubMedCentralCrossRef Aydemir O, Janko M, Hathaway NJ, Verity R, Mwandagalirwa MK, Tshefu AK, et al. Drug-resistance and population structure of Plasmodium falciparum across the Democratic Republic of Congo using high-throughput molecular inversion probes. J Infect Dis. 2018;218:946–55.PubMedPubMedCentralCrossRef
43.
go back to reference Arnaud-Haond S, Alberto F, Teixeira S, Procaccini G, Serr EA, Duarte CM. Assessing genetic diversity in clonal organisms: low diversity or low resolution? Combining power and cost efficiency in selecting markers. J Hered. 2005;96:434–40.PubMedCrossRef Arnaud-Haond S, Alberto F, Teixeira S, Procaccini G, Serr EA, Duarte CM. Assessing genetic diversity in clonal organisms: low diversity or low resolution? Combining power and cost efficiency in selecting markers. J Hered. 2005;96:434–40.PubMedCrossRef
44.
go back to reference Reusch TB. New markers- old questions: population genetics of seagrasses. Mar Ecol Prog Ser. 2001;211:261–74.CrossRef Reusch TB. New markers- old questions: population genetics of seagrasses. Mar Ecol Prog Ser. 2001;211:261–74.CrossRef
45.
go back to reference Miller RH, Hathaway NJ, Kharabora O, Mwandagalirwa K, Tshefu A, Meshnick SR, et al. A deep sequencing approach to estimate Plasmodium falciparum complexity of infection (COI) and explore apical membrane antigen 1 diversity. Malar J. 2017;16:490.PubMedPubMedCentralCrossRef Miller RH, Hathaway NJ, Kharabora O, Mwandagalirwa K, Tshefu A, Meshnick SR, et al. A deep sequencing approach to estimate Plasmodium falciparum complexity of infection (COI) and explore apical membrane antigen 1 diversity. Malar J. 2017;16:490.PubMedPubMedCentralCrossRef
46.
go back to reference Jalloh A, Jalloh M, Matsuoka H. T-cell epitope polymorphisms of the Plasmodium falciparum circumsporozoite protein among field isolates from Sierra Leone: age-dependent haplotype distribution? Malar J. 2009;8:120.PubMedPubMedCentralCrossRef Jalloh A, Jalloh M, Matsuoka H. T-cell epitope polymorphisms of the Plasmodium falciparum circumsporozoite protein among field isolates from Sierra Leone: age-dependent haplotype distribution? Malar J. 2009;8:120.PubMedPubMedCentralCrossRef
47.
go back to reference Chenet SM, Taylor JE, Blair S, Zuluaga L, Escalante AA. Longitudinal analysis of Plasmodium falciparum genetic variation in Turbo, Colombia: implications for malaria control and elimination. Malar J. 2015;14:363.PubMedPubMedCentralCrossRef Chenet SM, Taylor JE, Blair S, Zuluaga L, Escalante AA. Longitudinal analysis of Plasmodium falciparum genetic variation in Turbo, Colombia: implications for malaria control and elimination. Malar J. 2015;14:363.PubMedPubMedCentralCrossRef
48.
go back to reference Rice BL, Golden CD, Anjaranirina EJG, Botelho CM, Volkman SK, Hartl DL. Genetic evidence that the Makira region in northeastern Madagascar is a hotspot of malaria transmission. Malar J. 2016;15:596.PubMedPubMedCentralCrossRef Rice BL, Golden CD, Anjaranirina EJG, Botelho CM, Volkman SK, Hartl DL. Genetic evidence that the Makira region in northeastern Madagascar is a hotspot of malaria transmission. Malar J. 2016;15:596.PubMedPubMedCentralCrossRef
49.
go back to reference Ochola-Oyier LI, Okombo J, Wagatua N, Ochieng J, Tetteh KK, Fegan G, et al. Comparison of allele frequencies of Plasmodium falciparum merozoite antigens in malaria infections sampled in different years in a Kenyan population. Malar J. 2016;15:261.PubMedPubMedCentralCrossRef Ochola-Oyier LI, Okombo J, Wagatua N, Ochieng J, Tetteh KK, Fegan G, et al. Comparison of allele frequencies of Plasmodium falciparum merozoite antigens in malaria infections sampled in different years in a Kenyan population. Malar J. 2016;15:261.PubMedPubMedCentralCrossRef
50.
go back to reference Jones CM, Lee Y, Kitchen A, Collier T, Pringle JC, Muleba M, et al. Complete Anopheles funestus mitogenomes reveal an ancient history of mitochondrial lineages and their distribution in southern and central Africa. Sci Rep. 2018;8:9054.PubMedPubMedCentralCrossRef Jones CM, Lee Y, Kitchen A, Collier T, Pringle JC, Muleba M, et al. Complete Anopheles funestus mitogenomes reveal an ancient history of mitochondrial lineages and their distribution in southern and central Africa. Sci Rep. 2018;8:9054.PubMedPubMedCentralCrossRef
51.
go back to reference WHO. Malaria Policy Advisory Committee Meeting Evidence review group on border malaria Summary of conclusions and recommendations. Geneva: World Health Organization; 2018. WHO. Malaria Policy Advisory Committee Meeting Evidence review group on border malaria Summary of conclusions and recommendations. Geneva: World Health Organization; 2018.
52.
53.
go back to reference Gueye C, Teng A, Kinyua K, Wafula F, Gosling R, McCoy D. Parasites and vectors carry no passport: how to fund cross-border and regional efforts to achieve malaria elimination. Malar J. 2012;11:344.PubMedPubMedCentralCrossRef Gueye C, Teng A, Kinyua K, Wafula F, Gosling R, McCoy D. Parasites and vectors carry no passport: how to fund cross-border and regional efforts to achieve malaria elimination. Malar J. 2012;11:344.PubMedPubMedCentralCrossRef
Metadata
Title
High Plasmodium falciparum genetic diversity and temporal stability despite control efforts in high transmission settings along the international border between Zambia and the Democratic Republic of the Congo
Authors
Julia C. Pringle
Amy Wesolowski
Sophie Berube
Tamaki Kobayashi
Mary E. Gebhardt
Modest Mulenga
Mike Chaponda
Thierry Bobanga
Jonathan J. Juliano
Steven Meshnick
William J. Moss
Giovanna Carpi
Douglas E. Norris
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/s12936-019-3023-4

Other articles of this Issue 1/2019

Malaria Journal 1/2019 Go to the issue