Genetic evidence that the Makira region in northeastern Madagascar is a hotspot of malaria transmission

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Abstract

Background

Encouraging advances in the control of Plasmodium falciparum malaria have been observed across much of Africa in the past decade. However, regions of high relative prevalence and transmission that remain unaddressed or unrecognized provide a threat to this progress. Difficulties in identifying such localized hotspots include inadequate surveillance, especially in remote regions, and the cost and labor needed to produce direct estimates of transmission. Genetic data can provide a much-needed alternative to such empirical estimates, as the pattern of genetic variation within malaria parasite populations is indicative of the level of local transmission. Here, genetic data were used to provide the first empirical estimates of P. falciparum malaria prevalence and transmission dynamics for the rural, remote Makira region of northeastern Madagascar.

Methods

Longitudinal surveys of a cohort of 698 total individuals (both sexes, 0–74 years of age) were performed in two communities bordering the Makira Natural Park protected area. Rapid diagnostic tests, with confirmation by molecular methods, were used to estimate P. falciparum prevalence at three seasonal time points separated by 4-month intervals. Genomic loci in a panel of polymorphic, putatively neutral markers were genotyped for 94 P. falciparum infections and used to characterize genetic parameters known to correlate with transmission levels.

Results

Overall, 27.8% of individuals tested positive for P. falciparum over the 10-month course of the study, a rate approximately sevenfold higher than the countrywide average for Madagascar. Among those P. falciparum infections, a high level of genotypic diversity and a high frequency of polygenomic infections (68.1%) were observed, providing a pattern consistent with high and stable transmission.

Conclusions

Prevalence and genetic diversity data indicate that the Makira region is a hotspot of P. falciparum transmission in Madagascar. This suggests that the area should be highlighted for future interventions and that additional areas of high transmission may be present in ecologically similar regions nearby.

Electronic supplementary material

The online version of this article (doi:10.1186/s12936-016-1644-4) contains supplementary material, which is available to authorized users.

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Most cited references 28

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Identification of hot spots of malaria transmission for targeted malaria control.

Teun Bousema, Chris Drakeley, Samwel Gesase … (2010)

Variation in the risk of malaria within populations is a frequently described but poorly understood phenomenon. This heterogeneity creates opportunities for targeted interventions but only if hot spots of malaria transmission can be easily identified. We determined spatial patterns in malaria transmission in a district in northeastern Tanzania, using malaria incidence data from a cohort study involving infants and household-level mosquito sampling data. The parasite prevalence rates and age-specific seroconversion rates (SCRs) of antibodies against Plasmodium falciparum antigens were determined in samples obtained from people attending health care facilities. Five clusters of higher malaria incidence were detected and interpreted as hot spots of transmission. These hot spots partially overlapped with clusters of higher mosquito exposure but could not be satisfactorily predicted by a probability model based on environmental factors. Small-scale local variation in malaria exposure was detected by parasite prevalence rates and SCR estimates for samples of health care facility attendees. SCR estimates were strongly associated with local malaria incidence rates and predicted hot spots of malaria transmission with 95% sensitivity and 85% specificity. Serological markers were able to detect spatial variation in malaria transmission at the microepidemiological level, and they have the potential to form an effective method for spatial targeting of malaria control efforts.

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A general SNP-based molecular barcode for Plasmodium falciparum identification and tracking

Caroline Daniels, Sarah K Volkman, Danny A. Milner … (2008)

Background Single nucleotide polymorphism (SNP) genotyping provides the means to develop a practical, rapid, inexpensive assay that will uniquely identify any Plasmodium falciparum parasite using a small amount of DNA. Such an assay could be used to distinguish recrudescence from re-infection in drug trials, to monitor the frequency and distribution of specific parasites in a patient population undergoing drug treatment or vaccine challenge, or for tracking samples and determining purity of isolates in the laboratory during culture adaptation and sub-cloning, as well as routine passage. Methods A panel of twenty-four SNP markers has been identified that exhibit a high minor allele frequency (average MAF > 35%), for which robust TaqMan genotyping assays were constructed. All SNPs were identified through whole genome sequencing and MAF was estimated through Affymetrix array-based genotyping of a worldwide collection of parasites. These assays create a "molecular barcode" to uniquely identify a parasite genome. Results Using 24 such markers no two parasites known to be of independent origin have yet been found to have the same allele signature. The TaqMan genotyping assays can be performed on a variety of samples including cultured parasites, frozen whole blood, or whole blood spotted onto filter paper with a success rate > 99%. Less than 5 ng of parasite DNA is needed to complete a panel of 24 markers. The ability of this SNP panel to detect and identify parasites was compared to the standard molecular methods, MSP-1 and MSP-2 typing. Conclusion This work provides a facile field-deployable genotyping tool that can be used without special skills with standard lab equipment, and at reasonable cost that will unambiguously identify and track P. falciparum parasites both from patient samples and in the laboratory.

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Benefits of wildlife consumption to child nutrition in a biodiversity hotspot.

B Rasolofoniaina, Claire Kremen, D Golden … (2011)

Terrestrial wildlife is the primary source of meat for hundreds of millions of people throughout the developing world. Despite widespread human reliance on wildlife for food, the impact of wildlife depletion on human health remains poorly understood. Here we studied a prospective longitudinal cohort of 77 preadolescent children (under 12 y of age) in rural northeastern Madagascar and show that consuming more wildlife was associated with significantly higher hemoglobin concentrations. Our empirical models demonstrate that removing access to wildlife would induce a 29% increase in the numbers of children suffering from anemia and a tripling of anemia cases among children in the poorest households. The well-known progression from anemia to future disease demonstrates the powerful and far-reaching effects of lost wildlife access on a variety of human health outcomes, including cognitive, motor, and physical deficits. Loss of access to wildlife could arise either from the diligent enforcement of existing conservation policy or from unbridled unsustainable harvest, leading to depletion. Conservation enforcement would enact a more rapid restriction of resources, but self-depletion would potentially lead, albeit more slowly, both to irrevocable local wildlife extinctions and loss of the harvested resource. Our research quantifies costs of reduced access to wildlife for a rural community in Madagascar and illuminates pathways that may broadly link reduced natural resource access to declines in childhood health.

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Author and article information

Contributors

Benjamin L. Rice: benjaminrice@fas.harvard.edu

Christopher D. Golden: golden@hsph.harvard.edu

Evelin Jean Gasta Anjaranirina: charligasta03@gmail.com

Carolina Mastella Botelho: c.mastellabotelho@gmail.com

Sarah K. Volkman: c.mastellabotelho@gmail.com

Daniel L. Hartl: dhartl@oeb.harvard.edu

Journal

Journal ID (nlm-ta): Malar J

Journal ID (iso-abbrev): Malar. J

Title: Malaria Journal

Publisher: BioMed Central (London )

ISSN (Electronic): 1475-2875

Publication date (Electronic): 20 December 2016

Publication date PMC-release: 20 December 2016

Publication date Collection: 2016

Volume: 15

Electronic Location Identifier: 596

Affiliations

[1 ]Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA USA

[2 ]Department of Environmental Health, Harvard T.H. Chan School of Public Health, Boston, MA USA

[3 ]Harvard University Center for the Environment, Cambridge, MA USA

[4 ]Madagascar Health and Environmental Research (MAHERY), Maroantsetra, Madagascar

[5 ]Department of Pharmacy and Nutrition, Federal University of Espirito Santo, Alegre, ES Brazil

[6 ]Department of Immunology and Infectious Diseases, Harvard T.H. Chan School of Public Health, Boston, MA USA

Article

Publisher ID: 1644

DOI: 10.1186/s12936-016-1644-4

PMC ID: 5175380

PubMed ID: 27998292

SO-VID: dc9496c6-6c52-422f-b46b-3a1d40eaf56e

License:

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

History

Date received : 30 August 2016

Date accepted : 1 December 2016

Funding

Funded by: National Institutes of Health (US)

Award ID: AI106734

Award ID: AI099105

Award Recipient : Daniel L. Hartl

Funded by: The Rockefeller Foundation

Funded by: The Gordon and Betty Moore Foundation

Funded by: CAPES Foundation within the Ministry of Education, Brazil

Award ID: 88888.033957/2013-00

Award Recipient : Carolina Mastella Botelho

Custom metadata

ScienceOpen disciplines: Infectious disease & Microbiology

Keywords: madagascar,plasmodium falciparum,genetic diversity,genetic surveillance,polygenomic infections

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ScienceOpen disciplines: Infectious disease & Microbiology

Keywords: madagascar, plasmodium falciparum, genetic diversity, genetic surveillance, polygenomic infections

Genetic evidence that the Makira region in northeastern Madagascar is a hotspot of malaria transmission

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Background

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Malaria vaccine development

Most cited references 28

Identification of hot spots of malaria transmission for targeted malaria control.

A general SNP-based molecular barcode for Plasmodium falciparum identification and tracking

Benefits of wildlife consumption to child nutrition in a biodiversity hotspot.

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