Plasmodium falciparum Gametocyte Density and Infectivity in Peripheral Blood and Skin Tissue of Naturally Infected Parasite Carriers in Burkina Faso

Author:

Meibalan Elamaran12,Barry Aissata34,Gibbins Matthew P5,Awandu Shehu4,Meerstein-Kessel Lisette4,Achcar Fiona5,Bopp Selina1,Moxon Christopher5,Diarra Amidou3,Debe Siaka3,Ouédraogo Nicolas3,Barry-Some Ines3,Badoum Emilie S3,Fagnima Traoré6,Lanke Kjerstin4,Gonçalves Bronner P7,Bradley John8,Wirth Dyann1,Drakeley Chris7,Guelbeogo Wamdaogo Moussa3,Tiono Alfred B3,Marti Matthias15ORCID,Bousema Teun47ORCID

Affiliation:

1. Department of Immunology and Infectious Diseases, Harvard T.H. Chan School of Public Health, Boston, Massachusetts, USA

2. Center for Excellence in Vascular Biology, Department of Pathology, Brigham and Women’s Hospital, Boston, Massachusetts, USA

3. Centre National de Recherche et de Formation sur le Paludisme, Ouagadougou, Burkina Faso

4. Radboud Institute for Health Sciences, Radboud University Medical Center, the Netherlands

5. Wellcome Centre for Integrative Parasitology, Institute of Infection, Immunity and Inflammation, University of Glasgow, Glasgow, United Kingdom

6. Centre Hospitalier Universitaire Régional de Ouahigoua, Université de Ouahigouya, Burkina Faso

7. Immunology and Infection Department, London School of Hygiene and Tropical Medicine, London, United Kingdom

8. MRC Tropical Epidemiology Group, London School of Hygiene and Tropical Medicine, London, United Kingdom

Abstract

Abstract Background Plasmodium falciparum transmission depends on mature gametocytes that can be ingested by mosquitoes taking a blood meal on human skin. Although gametocyte skin sequestration has long been hypothesized as important contributor to efficient malaria transmission, this has never been formally tested. Methods In naturally infected gametocyte carriers from Burkina Faso, we assessed infectivity to mosquitoes by direct skin feeding and membrane feeding. We directly quantified male and female gametocytes and asexual parasites in finger-prick and venous blood samples, skin biopsy samples, and in of mosquitoes that fed on venous blood or directly on skin. Gametocytes were visualized in skin tissue with confocal microscopy. Results Although more mosquitoes became infected when feeding directly on skin then when feeding on venous blood (odds ratio, 2.01; 95% confidence interval, 1.21–3.33; P = .007), concentrations of gametocytes were not higher in the subdermal skin vasculature than in other blood compartments; only sparse gametocytes were observed in skin tissue. Discussion Our data strongly suggest that there is no significant skin sequestration of P. falciparum gametocytes. Gametocyte densities in peripheral blood are thus informative for predicting onward transmission potential to mosquitoes and can be used to target and monitor malaria elimination initiatives.

Funder

European Research Council

Bill and Melinda Gates Foundation

Netherlands Organization for Scientific Research

National Institutes of Health

Publisher

Oxford University Press (OUP)

Subject

Infectious Diseases,Immunology and Allergy

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