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


Journal

The Journal of infectious diseases
ISSN: 1537-6613
Titre abrégé: J Infect Dis
Pays: United States
ID NLM: 0413675

Informations de publication

Date de publication:
28 05 2021
Historique:
received: 14 10 2019
accepted: 23 12 2019
pubmed: 27 12 2019
medline: 12 2 2022
entrez: 27 12 2019
Statut: ppublish

Résumé

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.

Sections du résumé

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.

Identifiants

pubmed: 31875909
pii: 5687014
doi: 10.1093/infdis/jiz680
pmc: PMC8161640
doi:

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1822-1830

Subventions

Organisme : Medical Research Council
ID : MR/R010161/1
Pays : United Kingdom
Organisme : NIAID NIH HHS
ID : R21 AI117304
Pays : United States

Informations de copyright

© The Author(s) 2019. Published by Oxford University Press for the Infectious Diseases Society of America.

Références

Cell. 1995 Jul 14;82(1):77-87
pubmed: 7541722
Malar J. 2017 Aug 17;16(1):345
pubmed: 28818084
An Inst Med Trop (Lisb). 1952 Jun;9(2):553-62
pubmed: 13058140
Med Hypotheses. 2004;62(4):618-9
pubmed: 15050117
Sci Adv. 2018 May 23;4(5):eaat3775
pubmed: 29806032
Malar J. 2016 Sep 21;15(1):487
pubmed: 27653663
Blood. 2016 Jun 16;127(24):e42-53
pubmed: 27136945
Ann Soc Belg Med Trop (1920). 1952 Jun;32(3):209-11
pubmed: 12976890
Malar J. 2013 Feb 27;12:79
pubmed: 23442748
PLoS Negl Trop Dis. 2014 Jan 09;8(1):e2583
pubmed: 24416460
Trends Parasitol. 2018 Jan;34(1):64-79
pubmed: 28958602
Parasitology. 2003 Nov;127(Pt 5):427-35
pubmed: 14653532
Sci Transl Med. 2019 Jun 5;11(495):
pubmed: 31167926
Ann Soc Belg Med Trop (1920). 1948;28(2):273-7
pubmed: 18887719
Am J Trop Med Hyg. 2007 Aug;77(2):242-5
pubmed: 17690393
Nat Commun. 2017 Jul 5;8(1):57
pubmed: 28680146
PLoS One. 2012;7(8):e42821
pubmed: 22936993
J Infect Dis. 2017 Aug 15;216(4):457-467
pubmed: 28931236
Genome Med. 2015 Feb 27;7(1):19
pubmed: 25722744
Am J Trop Med Hyg. 2017 Jul;97(1):188-198
pubmed: 28719294
Front Immunol. 2019 Jan 14;9:3126
pubmed: 30692996
J Clin Invest. 2018 Apr 2;128(4):1551-1562
pubmed: 29389671
Mol Biochem Parasitol. 2009 Aug;166(2):93-8
pubmed: 19450726
Hum Vaccin Immunother. 2016 Dec;12(12):3189-3195
pubmed: 27184760
Elife. 2016 Sep 22;5:
pubmed: 27653219
Nature. 2015 Oct 8;526(7572):207-211
pubmed: 26375008
PLoS One. 2013 Sep 27;8(9):e76316
pubmed: 24312682
Blood. 2012 Jun 14;119(24):e172-80
pubmed: 22517905
Eukaryot Cell. 2011 Jun;10(6):744-52
pubmed: 21498641
Sci Transl Med. 2014 Jul 9;6(244):244re5
pubmed: 25009232
Nat Commun. 2017 Oct 26;8(1):1133
pubmed: 29074880
PLoS Med. 2017 Nov 30;14(11):e1002452
pubmed: 29190279
Lancet Infect Dis. 2016 Jun;16(6):674-684
pubmed: 26906747
Genome Med. 2014 Nov 29;6(11):110
pubmed: 25520756
Vaccine. 2016 Nov 21;34(48):5863-5870
pubmed: 27789147
Cell Microbiol. 2012 Jul;14(7):983-93
pubmed: 22417683
J Infect Dis. 2016 Jan 1;213(1):90-9
pubmed: 26142435

Auteurs

Elamaran Meibalan (E)

Department of Immunology and Infectious Diseases, Harvard T.H. Chan School of Public Health, Boston, Massachusetts, USA.
Center for Excellence in Vascular Biology, Department of Pathology, Brigham and Women's Hospital, Boston, Massachusetts, USA.

Aissata Barry (A)

Centre National de Recherche et de Formation sur le Paludisme, Ouagadougou, Burkina Faso.
Radboud Institute for Health Sciences, Radboud University Medical Center, the Netherlands.

Matthew P Gibbins (MP)

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

Shehu Awandu (S)

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

Lisette Meerstein-Kessel (L)

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

Fiona Achcar (F)

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

Selina Bopp (S)

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

Christopher Moxon (C)

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

Amidou Diarra (A)

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

Siaka Debe (S)

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

Nicolas Ouédraogo (N)

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

Ines Barry-Some (I)

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

Emilie S Badoum (ES)

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

Traoré Fagnima (T)

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

Kjerstin Lanke (K)

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

Bronner P Gonçalves (BP)

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

John Bradley (J)

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

Dyann Wirth (D)

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

Chris Drakeley (C)

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

Wamdaogo Moussa Guelbeogo (WM)

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

Alfred B Tiono (AB)

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

Matthias Marti (M)

Department of Immunology and Infectious Diseases, Harvard T.H. Chan School of Public Health, Boston, Massachusetts, USA.
Wellcome Centre for Integrative Parasitology, Institute of Infection, Immunity and Inflammation, University of Glasgow, Glasgow, United Kingdom.

Teun Bousema (T)

Radboud Institute for Health Sciences, Radboud University Medical Center, the Netherlands.
Immunology and Infection Department, London School of Hygiene and Tropical Medicine, London, United Kingdom.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH