Human Antibody Response to Anopheles gambiae Saliva: An Immuno-Epidemiological Biomarker to Evaluate the Efficacy of Insecticide-Treated Nets in Malaria Vector Control

Papa M. Drame Institut de Recherche pour le Développement (IRD), UR024 “Epidémiologie et Prévention” Unit, Dakar, Senegal; Institut de Recherche pour le Développement, UR016 “Contrôle et Caractérisation des Populations Vecteurs” Unit, Montpellier, France; Malaria Control Program, Société Nationale de Métallurgie (Sonamet), Lobito, Angola; Organisation de Coordination pour la Lutte contre les Endémies en Afrique (OCEAC), Laboratoire de Recherche sur le Paludisme, Yaoundé, Cameroun; Université Cheikh Anta Diop, Département de Biologie Animale, Dakar, Senegal; National Malaria Control Program, Ministry of Health, Luanda, Angola

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Anne Poinsignon Institut de Recherche pour le Développement (IRD), UR024 “Epidémiologie et Prévention” Unit, Dakar, Senegal; Institut de Recherche pour le Développement, UR016 “Contrôle et Caractérisation des Populations Vecteurs” Unit, Montpellier, France; Malaria Control Program, Société Nationale de Métallurgie (Sonamet), Lobito, Angola; Organisation de Coordination pour la Lutte contre les Endémies en Afrique (OCEAC), Laboratoire de Recherche sur le Paludisme, Yaoundé, Cameroun; Université Cheikh Anta Diop, Département de Biologie Animale, Dakar, Senegal; National Malaria Control Program, Ministry of Health, Luanda, Angola

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Patrick Besnard Institut de Recherche pour le Développement (IRD), UR024 “Epidémiologie et Prévention” Unit, Dakar, Senegal; Institut de Recherche pour le Développement, UR016 “Contrôle et Caractérisation des Populations Vecteurs” Unit, Montpellier, France; Malaria Control Program, Société Nationale de Métallurgie (Sonamet), Lobito, Angola; Organisation de Coordination pour la Lutte contre les Endémies en Afrique (OCEAC), Laboratoire de Recherche sur le Paludisme, Yaoundé, Cameroun; Université Cheikh Anta Diop, Département de Biologie Animale, Dakar, Senegal; National Malaria Control Program, Ministry of Health, Luanda, Angola

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Jacques Le Mire Institut de Recherche pour le Développement (IRD), UR024 “Epidémiologie et Prévention” Unit, Dakar, Senegal; Institut de Recherche pour le Développement, UR016 “Contrôle et Caractérisation des Populations Vecteurs” Unit, Montpellier, France; Malaria Control Program, Société Nationale de Métallurgie (Sonamet), Lobito, Angola; Organisation de Coordination pour la Lutte contre les Endémies en Afrique (OCEAC), Laboratoire de Recherche sur le Paludisme, Yaoundé, Cameroun; Université Cheikh Anta Diop, Département de Biologie Animale, Dakar, Senegal; National Malaria Control Program, Ministry of Health, Luanda, Angola

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Maria A. Dos-Santos Institut de Recherche pour le Développement (IRD), UR024 “Epidémiologie et Prévention” Unit, Dakar, Senegal; Institut de Recherche pour le Développement, UR016 “Contrôle et Caractérisation des Populations Vecteurs” Unit, Montpellier, France; Malaria Control Program, Société Nationale de Métallurgie (Sonamet), Lobito, Angola; Organisation de Coordination pour la Lutte contre les Endémies en Afrique (OCEAC), Laboratoire de Recherche sur le Paludisme, Yaoundé, Cameroun; Université Cheikh Anta Diop, Département de Biologie Animale, Dakar, Senegal; National Malaria Control Program, Ministry of Health, Luanda, Angola

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Cheikh S. Sow Institut de Recherche pour le Développement (IRD), UR024 “Epidémiologie et Prévention” Unit, Dakar, Senegal; Institut de Recherche pour le Développement, UR016 “Contrôle et Caractérisation des Populations Vecteurs” Unit, Montpellier, France; Malaria Control Program, Société Nationale de Métallurgie (Sonamet), Lobito, Angola; Organisation de Coordination pour la Lutte contre les Endémies en Afrique (OCEAC), Laboratoire de Recherche sur le Paludisme, Yaoundé, Cameroun; Université Cheikh Anta Diop, Département de Biologie Animale, Dakar, Senegal; National Malaria Control Program, Ministry of Health, Luanda, Angola

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Sylvie Cornelie Institut de Recherche pour le Développement (IRD), UR024 “Epidémiologie et Prévention” Unit, Dakar, Senegal; Institut de Recherche pour le Développement, UR016 “Contrôle et Caractérisation des Populations Vecteurs” Unit, Montpellier, France; Malaria Control Program, Société Nationale de Métallurgie (Sonamet), Lobito, Angola; Organisation de Coordination pour la Lutte contre les Endémies en Afrique (OCEAC), Laboratoire de Recherche sur le Paludisme, Yaoundé, Cameroun; Université Cheikh Anta Diop, Département de Biologie Animale, Dakar, Senegal; National Malaria Control Program, Ministry of Health, Luanda, Angola

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Vincent Foumane Institut de Recherche pour le Développement (IRD), UR024 “Epidémiologie et Prévention” Unit, Dakar, Senegal; Institut de Recherche pour le Développement, UR016 “Contrôle et Caractérisation des Populations Vecteurs” Unit, Montpellier, France; Malaria Control Program, Société Nationale de Métallurgie (Sonamet), Lobito, Angola; Organisation de Coordination pour la Lutte contre les Endémies en Afrique (OCEAC), Laboratoire de Recherche sur le Paludisme, Yaoundé, Cameroun; Université Cheikh Anta Diop, Département de Biologie Animale, Dakar, Senegal; National Malaria Control Program, Ministry of Health, Luanda, Angola

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Jean-Claude Toto Institut de Recherche pour le Développement (IRD), UR024 “Epidémiologie et Prévention” Unit, Dakar, Senegal; Institut de Recherche pour le Développement, UR016 “Contrôle et Caractérisation des Populations Vecteurs” Unit, Montpellier, France; Malaria Control Program, Société Nationale de Métallurgie (Sonamet), Lobito, Angola; Organisation de Coordination pour la Lutte contre les Endémies en Afrique (OCEAC), Laboratoire de Recherche sur le Paludisme, Yaoundé, Cameroun; Université Cheikh Anta Diop, Département de Biologie Animale, Dakar, Senegal; National Malaria Control Program, Ministry of Health, Luanda, Angola

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Mbacké Sembene Institut de Recherche pour le Développement (IRD), UR024 “Epidémiologie et Prévention” Unit, Dakar, Senegal; Institut de Recherche pour le Développement, UR016 “Contrôle et Caractérisation des Populations Vecteurs” Unit, Montpellier, France; Malaria Control Program, Société Nationale de Métallurgie (Sonamet), Lobito, Angola; Organisation de Coordination pour la Lutte contre les Endémies en Afrique (OCEAC), Laboratoire de Recherche sur le Paludisme, Yaoundé, Cameroun; Université Cheikh Anta Diop, Département de Biologie Animale, Dakar, Senegal; National Malaria Control Program, Ministry of Health, Luanda, Angola

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Denis Boulanger Institut de Recherche pour le Développement (IRD), UR024 “Epidémiologie et Prévention” Unit, Dakar, Senegal; Institut de Recherche pour le Développement, UR016 “Contrôle et Caractérisation des Populations Vecteurs” Unit, Montpellier, France; Malaria Control Program, Société Nationale de Métallurgie (Sonamet), Lobito, Angola; Organisation de Coordination pour la Lutte contre les Endémies en Afrique (OCEAC), Laboratoire de Recherche sur le Paludisme, Yaoundé, Cameroun; Université Cheikh Anta Diop, Département de Biologie Animale, Dakar, Senegal; National Malaria Control Program, Ministry of Health, Luanda, Angola

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François Simondon Institut de Recherche pour le Développement (IRD), UR024 “Epidémiologie et Prévention” Unit, Dakar, Senegal; Institut de Recherche pour le Développement, UR016 “Contrôle et Caractérisation des Populations Vecteurs” Unit, Montpellier, France; Malaria Control Program, Société Nationale de Métallurgie (Sonamet), Lobito, Angola; Organisation de Coordination pour la Lutte contre les Endémies en Afrique (OCEAC), Laboratoire de Recherche sur le Paludisme, Yaoundé, Cameroun; Université Cheikh Anta Diop, Département de Biologie Animale, Dakar, Senegal; National Malaria Control Program, Ministry of Health, Luanda, Angola

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Filomeno Fortes Institut de Recherche pour le Développement (IRD), UR024 “Epidémiologie et Prévention” Unit, Dakar, Senegal; Institut de Recherche pour le Développement, UR016 “Contrôle et Caractérisation des Populations Vecteurs” Unit, Montpellier, France; Malaria Control Program, Société Nationale de Métallurgie (Sonamet), Lobito, Angola; Organisation de Coordination pour la Lutte contre les Endémies en Afrique (OCEAC), Laboratoire de Recherche sur le Paludisme, Yaoundé, Cameroun; Université Cheikh Anta Diop, Département de Biologie Animale, Dakar, Senegal; National Malaria Control Program, Ministry of Health, Luanda, Angola

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Pierre Carnevale Institut de Recherche pour le Développement (IRD), UR024 “Epidémiologie et Prévention” Unit, Dakar, Senegal; Institut de Recherche pour le Développement, UR016 “Contrôle et Caractérisation des Populations Vecteurs” Unit, Montpellier, France; Malaria Control Program, Société Nationale de Métallurgie (Sonamet), Lobito, Angola; Organisation de Coordination pour la Lutte contre les Endémies en Afrique (OCEAC), Laboratoire de Recherche sur le Paludisme, Yaoundé, Cameroun; Université Cheikh Anta Diop, Département de Biologie Animale, Dakar, Senegal; National Malaria Control Program, Ministry of Health, Luanda, Angola

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Franck Remoue Institut de Recherche pour le Développement (IRD), UR024 “Epidémiologie et Prévention” Unit, Dakar, Senegal; Institut de Recherche pour le Développement, UR016 “Contrôle et Caractérisation des Populations Vecteurs” Unit, Montpellier, France; Malaria Control Program, Société Nationale de Métallurgie (Sonamet), Lobito, Angola; Organisation de Coordination pour la Lutte contre les Endémies en Afrique (OCEAC), Laboratoire de Recherche sur le Paludisme, Yaoundé, Cameroun; Université Cheikh Anta Diop, Département de Biologie Animale, Dakar, Senegal; National Malaria Control Program, Ministry of Health, Luanda, Angola

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For the fight against malaria, the World Health Organization (WHO) has emphasized the need for indicators to evaluate the efficacy of vector-control strategies. This study investigates a potential immunological marker, based on human antibody responses to Anopheles saliva, as a new indicator to evaluate the efficacy of insecticide-treated nets (ITNs). Parasitological, entomological, and immunological assessments were carried out in children and adults from a malaria-endemic region of Angola before and after the introduction of ITNs. Immunoglobulin G (IgG) levels to An. gambiae saliva were positively associated with the intensity of An. gambiae exposure and malaria infection. A significant decrease in the anti-saliva IgG response was observed after the introduction of ITNs, and this was associated with a drop in parasite load. This study represents the first stage in the development of a new indicator to evaluate the efficacy of malaria vector-control strategies, which could apply in other arthropod vector-borne diseases.

Author Notes

*Address correspondence to Papa Makhtar Drame, IRD/CREC, 01 BP 4414 RP, Cotonou, Bénin. E-mail: papa-makhtar.drame@ird.fr

Financial support: Papa M. Drame was supported by a fellowship provided by Institut de Recherche pour le Développement (IRD) (Département Soutien et Formation). Anne Poinsignon was supported by fellowships provided by the Research Ministry of France and François Lacoste. Sylvie Cornelie was supported by a fellowship from the Inkerman Foundation. This work was supported by Acer-Energy (Acergy)-Société Nationale de Métallurgie (Sonamet) Company (Malaria Control Program), the French Ministry of Defense (Délégation Générale pour l'Armement, DGA), and the IRD.

Authors' addresses: Papa Makhtar Drame, IRD/CREC, 01 BP 4414 RP, Cotonou, Bénin, E-mail: papa-makhtar.drame@ird.fr. Anne Poinsignon, IRD-UR016, BP 64501, 34394 Montpellier Cedex 5, France, E-mail: a.poinsignon@uq.edu.au. Patrick Besnard, Sonamet Company, 15 Rua 1° dezembro, CP 479, Lobito, Benguela Provincia, Angola, E-mail: prbesnard@yahoo.fr. Jacques Le Mire, Sonamet Company, 15 Rua 1° dezembro, CP 479, Lobito, Benguela Provincia, Angola, E-mail: drjlemire@yahoo.fr. Maria A. Dos-Santos, Sonamet Company, 15 Rua 1° dezembro, CP 479, Lobito, Benguela Provincia, Angola, E-mail: doctor.lobito@sonamet.com. Cheikh S. Sow, Espoir pour la Santé, St. Louis, Sénégal, E-mail: cheikh.sow@espoir-sante.org. Sylvie Cornélie, IRD-UR016, BP 64501, 34394 Montpellier Cedex 5, France, E-mail: sylvie.cornelie@ird.fr. Vincent Foumane, LRP-OCEAC, Yaoundé, Cameroun, E-mail: vfoumane@yahoo.fr. Jean-Claude Toto, LRP-OCEAC, Yaoundé, Cameroun, E-mail: jctotofr@yahoo.fr. Mbacké Sembène, Département de Biologie Animale, BP 5005, FST-UCAD, Dakar, Sénégal, E-mail: sembene@ird.sn. Denis Boulanger, IRD-UMR145, BP 64501, 34394 Montpellier Cedex 5, France, E-mail: denis.boulanger@ird.fr. Francois Simondon, IRD-UMR145, BP 64501, 34394 Montpellier Cedex 5, France, E-mail: FSimondon@spmsd.com. Filomeno Fortes, National Malaria Control Program, National Institute of Public Health, Ministry of Health, Luanda, Angola, E-mail: filomenofortes@gmail.com. Pierre Carnevale, IRD-UR016, BP 64501, 34394 Montpellier Cedex 5, France, E-mail: pjcarnevale@gmail.com. Franck Remoue, IRD/CREC, 01 BP 4414 RP, Cotonou, Bénin, E-mail: franck.remoue@ird.fr.

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