A non-destructive sugar-feeding assay for parasite detection and estimating the extrinsic incubation period of <i>Plasmodium falciparum</i> in individual mosquito vectors

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Abstract

Despite its epidemiological importance, the time Plasmodium parasites take to achieve development in the vector mosquito (the extrinsic incubation period, EIP) remains poorly characterized. A novel non-destructive assay designed to estimate EIP in single mosquitoes, and more broadly to study Plasmodium– Anopheles vectors interactions, is presented. The assay uses small pieces of cotton wool soaked in sugar solution to collect malaria sporozoites from individual mosquitoes during sugar feeding to monitor infection status over time. This technique has been tested across four natural malaria mosquito species of Africa and Asia, infected with Plasmodium falciparum (six field isolates from gametocyte-infected patients in Burkina Faso and the NF54 strain) and across a range of temperatures relevant to malaria transmission in field conditions. Monitoring individual infectious mosquitoes was feasible. The estimated median EIP of P. falciparum at 27 °C was 11 to 14 days depending on mosquito species and parasite isolate. Long-term individual tracking revealed that sporozoites transfer onto cotton wool can occur at least until day 40 post-infection. Short individual EIP were associated with short mosquito lifespan. Correlations between mosquito/parasite traits often reveal trade-offs and constraints and have important implications for understanding the evolution of parasite transmission strategies.

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Insertion polymorphisms of SINE200 retrotransposons within speciation islands of Anopheles gambiae molecular forms

Federica Santolamazza, Emiliano Mancini, Frédéric Simard … (2008)

Background SINEs (Short INterspersed Elements) are homoplasy-free and co-dominant genetic markers which are considered to represent useful tools for population genetic studies, and could help clarifying the speciation processes ongoing within the major malaria vector in Africa, Anopheles gambiae s.s. Here, we report the results of the analysis of the insertion polymorphism of a nearly 200 bp-long SINE (SINE200) within genome areas of high differentiation (i.e. "speciation islands") of M and S A. gambiae molecular forms. Methods A SINE-PCR approach was carried out on thirteen SINE200 insertions in M and S females collected along the whole range of distribution of A. gambiae s.s. in sub-Saharan Africa. Ten specimens each for Anopheles arabiensis, Anopheles melas, Anopheles quadriannulatus A and 15 M/S hybrids from laboratory crosses were also analysed. Results Eight loci were successfully amplified and were found to be specific for A. gambiae s.s.: 5 on 2L chromosome and one on X chromosome resulted monomorphic, while two loci positioned respectively on 2R (i.e. S200 2R12D) and X (i.e. S200 X6.1) chromosomes were found to be polymorphic. S200 2R12D was homozygote for the insertion in most S-form samples, while intermediate levels of polymorphism were shown in M-form, resulting in an overall high degree of genetic differentiation between molecular forms (Fst = 0.46 p < 0.001) and within M-form (Fst = 0.46 p < 0.001). The insertion of S200 X6.1 was found to be fixed in all M- and absent in all S-specimens. This led to develop a novel easy-to-use PCR approach to straightforwardly identify A. gambiae molecular forms. This novel approach allows to overcome the constraints associated with markers on the rDNA region commonly used for M and S identification. In fact, it is based on a single copy and irreversible SINE200 insertion and, thus, is not subjected to peculiar evolutionary patterns affecting rDNA markers, e.g. incomplete homogenization of the arrays through concerted evolution and/or mixtures of M and S IGS-sequences among the arrays of single chromatids. Conclusion The approach utilized allowed to develop new easy-to-use co-dominant markers for the analysis of genetic differentiation between M and S-forms and opens new perspectives in the study of the speciation process ongoing within A. gambiae.

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Vectorial capacity and vector control: reconsidering sensitivity to parameters for malaria elimination

Oliver J Brady, H. Godfray, Andrew Tatem … (2016)

Background Major gains have been made in reducing malaria transmission in many parts of the world, principally by scaling-up coverage with long-lasting insecticidal nets and indoor residual spraying. Historically, choice of vector control intervention has been largely guided by a parameter sensitivity analysis of George Macdonald's theory of vectorial capacity that suggested prioritizing methods that kill adult mosquitoes. While this advice has been highly successful for transmission suppression, there is a need to revisit these arguments as policymakers in certain areas consider which combinations of interventions are required to eliminate malaria. Methods and Results Using analytical solutions to updated equations for vectorial capacity we build on previous work to show that, while adult killing methods can be highly effective under many circumstances, other vector control methods are frequently required to fill effective coverage gaps. These can arise due to pre-existing or developing mosquito physiological and behavioral refractoriness but also due to additive changes in the relative importance of different vector species for transmission. Furthermore, the optimal combination of interventions will depend on the operational constraints and costs associated with reaching high coverage levels with each intervention. Conclusions Reaching specific policy goals, such as elimination, in defined contexts requires increasingly non-generic advice from modelling. Our results emphasize the importance of measuring baseline epidemiology, intervention coverage, vector ecology and program operational constraints in predicting expected outcomes with different combinations of interventions.

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Influence of climate on malaria transmission depends on daily temperature variation.

Matthew B. Thomas, Krijn Paaijmans, Justine I. Blanford … (2010)

Malaria transmission is strongly influenced by environmental temperature, but the biological drivers remain poorly quantified. Most studies analyzing malaria-temperature relations, including those investigating malaria risk and the possible impacts of climate change, are based solely on mean temperatures and extrapolate from functions determined under unrealistic laboratory conditions. Here, we present empirical evidence to show that, in addition to mean temperatures, daily fluctuations in temperature affect parasite infection, the rate of parasite development, and the essential elements of mosquito biology that combine to determine malaria transmission intensity. In general, we find that, compared with rates at equivalent constant mean temperatures, temperature fluctuation around low mean temperatures acts to speed up rate processes, whereas fluctuation around high mean temperatures acts to slow processes down. At the extremes (conditions representative of the fringes of malaria transmission, where range expansions or contractions will occur), fluctuation makes transmission possible at lower mean temperatures than currently predicted and can potentially block transmission at higher mean temperatures. If we are to optimize control efforts and develop appropriate adaptation or mitigation strategies for future climates, we need to incorporate into predictive models the effects of daily temperature variation and how that variation is altered by climate change.

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Author and article information

Contributors

Edwige Guissou: edwigeguissou@yahoo.fr

Journal

Journal ID (nlm-ta): Sci Rep

Journal ID (iso-abbrev): Sci Rep

Title: Scientific Reports

Publisher: Nature Publishing Group UK (London )

ISSN (Electronic): 2045-2322

Publication date (Electronic): 29 April 2021

Publication date PMC-release: 29 April 2021

Publication date Collection: 2021

Volume: 11

Electronic Location Identifier: 9344

Affiliations

[1 ]GRID grid.457337.1, ISNI 0000 0004 0564 0509, Institut de Recherche en Sciences de la Santé, ; Bobo-Dioulasso, Burkina Faso

[2 ]GRID grid.462603.5, ISNI 0000 0004 0382 3424, MIVEGEC, Montpellier University, IRD, CNRS, ; Montpellier, France

[3 ]Laboratoire mixte international sur les vecteurs (LAMIVECT), Bobo Dioulasso, Burkina Faso

[4 ]GRID grid.442667.5, ISNI 0000 0004 0474 2212, Université Nazi Boni, ; Bobo Dioulasso, Burkina Faso

[5 ]GRID grid.29857.31, ISNI 0000 0001 2097 4281, Center for Infectious Disease Dynamics, , The Pennsylvania State University, ; University Park, PA 16802 USA

[6 ]Green Mountain Antibodies, Inc. 1 Mill St. Suites 1-7, Burlington, VT 05401 USA

[7 ]GRID grid.5685.e, ISNI 0000 0004 1936 9668, York Environmental Sustainability Institute and Department of Biology, , University of York, ; York, UK

[8 ]Centre de Recherche en Écologie et Évolution de la Santé (CREES), Montpellier, France

Article

Publisher ID: 88659

DOI: 10.1038/s41598-021-88659-w

PMC ID: 8085177

PubMed ID: 33927245

SO-VID: 97c625b7-bdbd-4bf7-aaef-ed7ac5163c47

License:

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

History

Date received : 12 January 2021

Date accepted : 14 April 2021

Funding

Funded by: IRD LMI LAMIVECT incentive grant

Award ID: EG2017

Funded by: NIH NIAID grant

Award ID: # R01AI110793

Funded by: National Science Foundation Ecology and Evolution of Infectious Diseases grant

Award ID: DEB-1518681

Funded by: ANR grant

Award ID: nos.11-PDOC-006-01

Award ID: 16-CE35-0007

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ScienceOpen disciplines: Uncategorized

Keywords: ecology,evolution,molecular biology,zoology,medical research,diseases,infectious diseases

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ScienceOpen disciplines: Uncategorized

Keywords: ecology, evolution, molecular biology, zoology, medical research, diseases, infectious diseases

A non-destructive sugar-feeding assay for parasite detection and estimating the extrinsic incubation period of Plasmodium falciparum in individual mosquito vectors

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Abstract

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Point-of-Care Testing for Infectious Diseases Super Collection

Most cited references 46

Insertion polymorphisms of SINE200 retrotransposons within speciation islands of Anopheles gambiae molecular forms

Vectorial capacity and vector control: reconsidering sensitivity to parameters for malaria elimination

Influence of climate on malaria transmission depends on daily temperature variation.

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