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Distinctive genetic structure and selection patterns in Plasmodium vivax from South Asia and East Africa.

ABSTRACT: Despite the high burden of Plasmodium vivax malaria in South Asian countries, the genetic diversity of circulating parasite populations is not well described. Determinants of antimalarial drug susceptibility for P. vivax in the region have not been characterised. Our genomic analysis of global P. vivax (n = 558) establishes South Asian isolates (n = 92) as a distinct subpopulation, which shares ancestry with some East African and South East Asian parasites. Signals of positive selection are linked to drug resistance-associated loci including pvkelch10, pvmrp1, pvdhfr and pvdhps, and two loci linked to P. vivax invasion of reticulocytes, pvrbp1a and pvrbp1b. Significant identity-by-descent was found in extended chromosome regions common to P. vivax from India and Ethiopia, including the pvdbp gene associated with Duffy blood group binding. Our investigation provides new understanding of global P. vivax population structure and genomic diversity, and genetic evidence of recent directional selection in this important human pathogen.

SUBMITTER: Benavente ED

PROVIDER: S-EPMC8154914 | biostudies-literature | 2021 May

REPOSITORIES: biostudies-literature

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Distinctive genetic structure and selection patterns in Plasmodium vivax from South Asia and East Africa.

Benavente Ernest Diez ED Manko Emilia E Phelan Jody J Campos Monica M Nolder Debbie D Fernandez Diana D Velez-Tobon Gabriel G Castaño Alberto Tobón AT Dombrowski Jamille G JG Marinho Claudio R F CRF Aguiar Anna Caroline C ACC Pereira Dhelio Batista DB Sriprawat Kanlaya K Nosten Francois F Moon Robert R Sutherland Colin J CJ Campino Susana S Clark Taane G TG

Nature communications 20210526 1

Despite the high burden of Plasmodium vivax malaria in South Asian countries, the genetic diversity of circulating parasite populations is not well described. Determinants of antimalarial drug susceptibility for P. vivax in the region have not been characterised. Our genomic analysis of global P. vivax (n = 558) establishes South Asian isolates (n = 92) as a distinct subpopulation, which shares ancestry with some East African and South East Asian parasites. Signals of positive selection are link ...[more]

PMID: 34039976

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Project description:BACKGROUND:Parasite genetic diversity and multiplicity of infection (MOI) affect clinical outcomes, response to drug treatment and naturally-acquired or vaccine-induced immunity. Traditional methods often underestimate the frequency and diversity of multiclonal infections due to technical sensitivity and specificity. Next-generation sequencing techniques provide a novel opportunity to study complexity of parasite populations and molecular epidemiology. METHODS:Symptomatic and asymptomatic Plasmodium vivax samples were collected from health centres/hospitals and schools, respectively, from 2011 to 2015 in Ethiopia. Similarly, both symptomatic and asymptomatic Plasmodium falciparum samples were collected, respectively, from hospitals and schools in 2005 and 2015 in Kenya. Finger-pricked blood samples were collected and dried on filter paper. Long amplicon (> 400 bp) deep sequencing of merozoite surface protein 1 (msp1) gene was conducted to determine multiplicity and molecular epidemiology of P. vivax and P. falciparum infections. The results were compared with those based on short amplicon (117 bp) deep sequencing. RESULTS:A total of 139 P. vivax and 222 P. falciparum samples were pyro-sequenced for pvmsp1 and pfmsp1, yielding a total of 21 P. vivax and 99 P. falciparum predominant haplotypes. The average MOI for P. vivax and P. falciparum were 2.16 and 2.68, respectively, which were significantly higher than that of microsatellite markers and short amplicon (117 bp) deep sequencing. Multiclonal infections were detected in 62.2% of the samples for P. vivax and 74.8% of the samples for P. falciparum. Four out of the five subjects with recurrent P. vivax malaria were found to be a relapse 44-65 days after clearance of parasites. No difference was observed in MOI among P. vivax patients of different symptoms, ages and genders. Similar patterns were also observed in P. falciparum except for one study site in Kenyan lowland areas with significantly higher MOI. CONCLUSIONS:The study used a novel method to evaluate Plasmodium MOI and molecular epidemiological patterns by long amplicon ultra-deep sequencing. The complexity of infections were similar among age groups, symptoms, genders, transmission settings (spatial heterogeneity), as well as over years (pre- vs. post-scale-up interventions). This study demonstrated that long amplicon deep sequencing is a useful tool to investigate multiplicity and molecular epidemiology of Plasmodium parasite infections.

Project description:Malaria in sub-Saharan Africa has historically been almost exclusively attributed to Plasmodium falciparum (Pf). Current diagnostic and surveillance systems in much of sub-Saharan Africa are not designed to identify or report non-Pf human malaria infections accurately, resulting in a dearth of routine epidemiological data about their significance. The high prevalence of Duffy negativity provided a rationale for excluding the possibility of Plasmodium vivax (Pv) transmission. However, review of varied evidence sources including traveller infections, community prevalence surveys, local clinical case reports, entomological and serological studies contradicts this viewpoint. Here, these data reports are weighted in a unified framework to reflect the strength of evidence of indigenous Pv transmission in terms of diagnostic specificity, size of individual reports and corroboration between evidence sources. Direct evidence was reported from 21 of the 47 malaria-endemic countries studied, while 42 countries were attributed with infections of visiting travellers. Overall, moderate to conclusive evidence of transmission was available from 18 countries, distributed across all parts of the continent. Approximately 86.6 million Duffy positive hosts were at risk of infection in Africa in 2015. Analysis of the mechanisms sustaining Pv transmission across this continent of low frequency of susceptible hosts found that reports of Pv prevalence were consistent with transmission being potentially limited to Duffy positive populations. Finally, reports of apparent Duffy-independent transmission are discussed. While Pv is evidently not a major malaria parasite across most of sub-Saharan Africa, the evidence presented here highlights its widespread low-level endemicity. An increased awareness of Pv as a potential malaria parasite, coupled with policy shifts towards species-specific diagnostics and reporting, will allow a robust assessment of the public health significance of Pv, as well as the other neglected non-Pf parasites, which are currently invisible to most public health authorities in Africa, but which can cause severe clinical illness and require specific control interventions.

Project description:Understanding major climate risks, adaptation strategies, and factors influencing the choice of those strategies is crucial to reduce farmers' vulnerability. Employing comprehensive data from 2822 farm households in Ethiopia and Kenya (East Africa; EA) and 1902 farm households in Bangladesh, India, and Nepal (South Asia; SA), this study investigates the main climate risks that farmers faced and the adaptation strategies they used. Among others, excessive rainfall and heightened crop pest/disease incidence are commonly observed climate-induced risks in all study areas, while cyclones and salinity are unique to Bangladesh. Drought is prevalent in Ethiopia, India, Kenya, and Nepal. Farmers in those countries responded with strategies that include change in farming practices, sustainable land management, reduce consumption, sell assets, use savings and borrowings, seek alternative employment and assistance from government or NGO. In general, farmers faced several multiple climate risks simultaneously and they responded with multiple adaptation strategies. Therefore, this study used a multivariate probit (MVP) approach to examine the factors influencing the adoption of adaptation strategies. Unlike other studies, we also tested and corrected for possible endogeneity in model estimation. All the countries mentioned have low adaptive capacity to address climate change, which is further weakened by inadequate governance and inefficient institutions. We observed significant differences in the choice of adaptation strategies between male-headed households (MHHs) and female-headed households (FHHs), as well as across countries. Generally, MHHs are more likely to seek additional employment and change agricultural practices, while FHHs and households headed by older persons tend to reduce consumption and rely on savings and borrowings. Institutional support for adaptation is much less in EA compared to SA. Training on alternative farming practices, enhancing non-farm employment options, better institutional support, and social security for older farmers are crucial for climate change adaptation in both regions.

Dataset Information

Distinctive genetic structure and selection patterns in Plasmodium vivax from South Asia and East Africa.

Publications

Distinctive genetic structure and selection patterns in Plasmodium vivax from South Asia and East Africa.

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