Infectiousness of the Human Population to Anopheles arabiensis by Direct Skin Feeding in an Area Hypoendemic for Malaria in Senegal

Abdoulaye Gaye Unité de Recherche sur les Maladies Infectieuses et Tropicales Emergentes, UMR 198, Campus UCAD – IRD, BP 1386, Dakar, Sénégal; Department of Medical Microbiology, Radboud University Medical Center, Nijmegen, The Netherlands; Department of Immunology and Infection, London School of Hygiene and Tropical Medicine, London, United Kingdom; Programme Nationale de Lutte Contre le Paludisme, Dakar-Fann Sénégal; Institut Pasteur de Bangui, République Centrafricaine; Universite Cheikh Anta Diop de Dakar, Departement de Biologie Animale, Dakar – Sénégal; Medical Research Council Unit, Banjul; Atlantic Boulevard Fajara, Fajara, The Gambia

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Teun Bousema Unité de Recherche sur les Maladies Infectieuses et Tropicales Emergentes, UMR 198, Campus UCAD – IRD, BP 1386, Dakar, Sénégal; Department of Medical Microbiology, Radboud University Medical Center, Nijmegen, The Netherlands; Department of Immunology and Infection, London School of Hygiene and Tropical Medicine, London, United Kingdom; Programme Nationale de Lutte Contre le Paludisme, Dakar-Fann Sénégal; Institut Pasteur de Bangui, République Centrafricaine; Universite Cheikh Anta Diop de Dakar, Departement de Biologie Animale, Dakar – Sénégal; Medical Research Council Unit, Banjul; Atlantic Boulevard Fajara, Fajara, The Gambia

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Gadiaga Libasse Unité de Recherche sur les Maladies Infectieuses et Tropicales Emergentes, UMR 198, Campus UCAD – IRD, BP 1386, Dakar, Sénégal; Department of Medical Microbiology, Radboud University Medical Center, Nijmegen, The Netherlands; Department of Immunology and Infection, London School of Hygiene and Tropical Medicine, London, United Kingdom; Programme Nationale de Lutte Contre le Paludisme, Dakar-Fann Sénégal; Institut Pasteur de Bangui, République Centrafricaine; Universite Cheikh Anta Diop de Dakar, Departement de Biologie Animale, Dakar – Sénégal; Medical Research Council Unit, Banjul; Atlantic Boulevard Fajara, Fajara, The Gambia

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Mamadou O. Ndiath Unité de Recherche sur les Maladies Infectieuses et Tropicales Emergentes, UMR 198, Campus UCAD – IRD, BP 1386, Dakar, Sénégal; Department of Medical Microbiology, Radboud University Medical Center, Nijmegen, The Netherlands; Department of Immunology and Infection, London School of Hygiene and Tropical Medicine, London, United Kingdom; Programme Nationale de Lutte Contre le Paludisme, Dakar-Fann Sénégal; Institut Pasteur de Bangui, République Centrafricaine; Universite Cheikh Anta Diop de Dakar, Departement de Biologie Animale, Dakar – Sénégal; Medical Research Council Unit, Banjul; Atlantic Boulevard Fajara, Fajara, The Gambia

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Lassana Konaté Unité de Recherche sur les Maladies Infectieuses et Tropicales Emergentes, UMR 198, Campus UCAD – IRD, BP 1386, Dakar, Sénégal; Department of Medical Microbiology, Radboud University Medical Center, Nijmegen, The Netherlands; Department of Immunology and Infection, London School of Hygiene and Tropical Medicine, London, United Kingdom; Programme Nationale de Lutte Contre le Paludisme, Dakar-Fann Sénégal; Institut Pasteur de Bangui, République Centrafricaine; Universite Cheikh Anta Diop de Dakar, Departement de Biologie Animale, Dakar – Sénégal; Medical Research Council Unit, Banjul; Atlantic Boulevard Fajara, Fajara, The Gambia

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Musa Jawara Unité de Recherche sur les Maladies Infectieuses et Tropicales Emergentes, UMR 198, Campus UCAD – IRD, BP 1386, Dakar, Sénégal; Department of Medical Microbiology, Radboud University Medical Center, Nijmegen, The Netherlands; Department of Immunology and Infection, London School of Hygiene and Tropical Medicine, London, United Kingdom; Programme Nationale de Lutte Contre le Paludisme, Dakar-Fann Sénégal; Institut Pasteur de Bangui, République Centrafricaine; Universite Cheikh Anta Diop de Dakar, Departement de Biologie Animale, Dakar – Sénégal; Medical Research Council Unit, Banjul; Atlantic Boulevard Fajara, Fajara, The Gambia

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Ousmane Faye Unité de Recherche sur les Maladies Infectieuses et Tropicales Emergentes, UMR 198, Campus UCAD – IRD, BP 1386, Dakar, Sénégal; Department of Medical Microbiology, Radboud University Medical Center, Nijmegen, The Netherlands; Department of Immunology and Infection, London School of Hygiene and Tropical Medicine, London, United Kingdom; Programme Nationale de Lutte Contre le Paludisme, Dakar-Fann Sénégal; Institut Pasteur de Bangui, République Centrafricaine; Universite Cheikh Anta Diop de Dakar, Departement de Biologie Animale, Dakar – Sénégal; Medical Research Council Unit, Banjul; Atlantic Boulevard Fajara, Fajara, The Gambia

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Cheikh Sokhna Unité de Recherche sur les Maladies Infectieuses et Tropicales Emergentes, UMR 198, Campus UCAD – IRD, BP 1386, Dakar, Sénégal; Department of Medical Microbiology, Radboud University Medical Center, Nijmegen, The Netherlands; Department of Immunology and Infection, London School of Hygiene and Tropical Medicine, London, United Kingdom; Programme Nationale de Lutte Contre le Paludisme, Dakar-Fann Sénégal; Institut Pasteur de Bangui, République Centrafricaine; Universite Cheikh Anta Diop de Dakar, Departement de Biologie Animale, Dakar – Sénégal; Medical Research Council Unit, Banjul; Atlantic Boulevard Fajara, Fajara, The Gambia

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Direct skin feeding experiments are sensitive assays to determine human infectiousness to mosquitoes but are rarely used in malaria epidemiological surveys. We determined the infectiousness of inhabitants of a malaria hypoendemic area in Senegal. Gametocyte prevalence by microscopy was 13.5% (26 of 192). Of all individuals who were gametocyte positive, 44.4% (11 of 25) infected ≥ 1 Anopheles arabiensis mosquito and 10.8% (54 of 500) of mosquitoes became infected. Of all individuals who were gametocyte negative by microscopy, 4.3% (7 of 162) infected ≥ 1 mosquito and 0.4% (12 of 3240) of mosquitoes became infected. The 18.2% (12 of 66) of all mosquito infections was a result of submicroscopic gametocyte carriage and two individuals without asexual parasites or gametocytes by microscopy were infectious to mosquitoes. When infectivity and local demography was taken into account, children 5–14 years of age contributed 50.8% of the human infectious reservoir for malaria. Adults and submicroscopic gametocyte carriers may contribute considerably to onward malaria transmission in our setting.

Author Notes

* Address correspondence to Abdoulaye Gaye, Medical Research Council Unit, The Gambia, Atlantic Boulevard, Fajara, P.O. Box 273, Banjul, Basse, The Gambia. E-mail: layegaye@gmail.com

Financial support: This work was supported by the Institute of Research for Development (IRD).

Authors' addresses: Abdoulaye Gaye and Musa Jawara, Medical Research Council Unit, Banjul, Fajara, The Gambia, E-mails: abgaye@mrc.gm/layegaye@gmail.com and jawaramusa@mrc.gm. Teun Bousema, Department of Medical Microbiology, Radboud University Medical Center, Nijmegen, The Netherlands; Department of Immunology and Infection, London School of Hygiene and Tropical Medicine, London, UK, E-mail: Teun.Bousema@lshtm.ac.uk. Gadiaga Libasse, Programme Nationale de Lutte contre le Paludisme, Dakar-Fann, Sénégal, E-mail: lgadius@gmail.com. Mamadou O. Ndiath, Institut Pasteur de Bangui, République Centrafricaine, E-mail: ousmane.ndiath@gmail.com. Lassana Konaté and Ousmane Faye, Universite Cheikh Anta Diop de Dakar, Departement de Biologie Animale, Dakar, Senegal, E-mails: konatela@yahoo.fr and jogomaye@yahoo.fr. Cheikh Sokhna, Unite de Recherche sur les Maladies Infectieuses et Tropicales Emergentes, UMR 198, Campus UCAD – IRD, Dakar, Senegal, E-mail: cheikh.sokhna@ird.fr.

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