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

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...

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Published inThe Journal of infectious diseases Vol. 223; no. 10; pp. 1822 - 1830
Main Authors Meibalan, Elamaran, Barry, Aissata, Gibbins, Matthew P, Awandu, Shehu, Meerstein-Kessel, Lisette, Achcar, Fiona, Bopp, Selina, Moxon, Christopher, Diarra, Amidou, Debe, Siaka, Ouédraogo, Nicolas, Barry-Some, Ines, Badoum, Emilie S, Fagnima, Traoré, Lanke, Kjerstin, Gonçalves, Bronner P, Bradley, John, Wirth, Dyann, Drakeley, Chris, Guelbeogo, Wamdaogo Moussa, Tiono, Alfred B, Marti, Matthias, Bousema, Teun
Format Journal Article
LanguageEnglish
Published US Oxford University Press 28.05.2021
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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. Plasmodium falciparum gametocyte skin sequestration has long been hypothesized but never formally tested. We observed no evidence for higher gametocyte densities in skin tissue of naturally infected gametocyte carriers or blood meals of mosquitoes feeding on their skin.
AbstractList 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. 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. 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. 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.
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.
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.
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. Plasmodium falciparum gametocyte skin sequestration has long been hypothesized but never formally tested. We observed no evidence for higher gametocyte densities in skin tissue of naturally infected gametocyte carriers or blood meals of mosquitoes feeding on their skin.
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.BACKGROUNDPlasmodium 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.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.METHODSIn 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.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.RESULTSAlthough 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.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.DISCUSSIONOur 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.
Plasmodium falciparum gametocyte skin sequestration has long been hypothesized but never formally tested. We observed no evidence for higher gametocyte densities in skin tissue of naturally infected gametocyte carriers or blood meals of mosquitoes feeding on their skin.
Author Meerstein-Kessel, Lisette
Bousema, Teun
Bopp, Selina
Tiono, Alfred B
Wirth, Dyann
Gonçalves, Bronner P
Badoum, Emilie S
Moxon, Christopher
Achcar, Fiona
Barry, Aissata
Gibbins, Matthew P
Guelbeogo, Wamdaogo Moussa
Diarra, Amidou
Fagnima, Traoré
Ouédraogo, Nicolas
Bradley, John
Drakeley, Chris
Awandu, Shehu
Marti, Matthias
Debe, Siaka
Barry-Some, Ines
Lanke, Kjerstin
Meibalan, Elamaran
AuthorAffiliation 5 Wellcome Centre for Integrative Parasitology, Institute of Infection, Immunity and Inflammation, University of Glasgow , Glasgow , United Kingdom
2 Center for Excellence in Vascular Biology, Department of Pathology, Brigham and Women’s Hospital , Boston, Massachusetts , USA
7 Immunology and Infection Department, London School of Hygiene and Tropical Medicine , London , United Kingdom
1 Department of Immunology and Infectious Diseases, Harvard T.H. Chan School of Public Health , Boston, Massachusetts , USA
4 Radboud Institute for Health Sciences, Radboud University Medical Center , the Netherlands
3 Centre National de Recherche et de Formation sur le Paludisme , Ouagadougou , Burkina Faso
6 Centre Hospitalier Universitaire Régional de Ouahigoua, Université de Ouahigouya , Burkina Faso
8 MRC Tropical Epidemiology Group, London School of Hygiene and Tropical Medicine , London , United Kingdom
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ContentType Journal Article
Copyright The Author(s) 2019. Published by Oxford University Press for the Infectious Diseases Society of America. 2019
The Author(s) 2019. Published by Oxford University Press for the Infectious Diseases Society of America.
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Issue 10
Keywords gametocyte
transmission
anopheles
elimination
sequestration
Plasmodium falciparum
Language English
License This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
The Author(s) 2019. Published by Oxford University Press for the Infectious Diseases Society of America.
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content type line 23
E. M., A. B., and M. P. G. contributed equally to this work.
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Snippet Abstract Background Plasmodium falciparum transmission depends on mature gametocytes that can be ingested by mosquitoes taking a blood meal on human skin....
Plasmodium falciparum transmission depends on mature gametocytes that can be ingested by mosquitoes taking a blood meal on human skin. Although gametocyte skin...
Background Plasmodium falciparum transmission depends on mature gametocytes that can be ingested by mosquitoes taking a blood meal on human skin. Although...
Plasmodium falciparum gametocyte skin sequestration has long been hypothesized but never formally tested. We observed no evidence for higher gametocyte...
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StartPage 1822
SubjectTerms Animals
Anopheles - parasitology
Biopsy
Burkina Faso
Confocal microscopy
Culicidae
Disease transmission
Feeding
Gametocytes
Humans
Infectivity
Major and Brief Reports
Malaria
Malaria, Falciparum - epidemiology
Mosquitoes
Peripheral blood
Plasmodium falciparum
Skin
Title Plasmodium falciparum Gametocyte Density and Infectivity in Peripheral Blood and Skin Tissue of Naturally Infected Parasite Carriers in Burkina Faso
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