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Reference Manager
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The Impact of Periodic Distribution Campaigns of Long-Lasting Insecticidal-Treated Bed Nets on Malaria Vector Dynamics and Human Exposure in Dielmo, Senegal
Seynabou Sougoufara
Seynabou Sougoufara
Aix Marseille University, Institut de Recherche pour le Développement (IDR) (Dakar, Marseille, Papeete), AP-HM, Institut Hospitalo-Universitaire-Méditerranée Infection, UMR Vecteurs—Infections Tropicales et Méditerranéennes (VITROME), Marseille, France;
Département de Biologie Animale, Faculté des Sciences et Techniques, Université Cheikh Anta Diop de Dakar, Dakar Fann, Sénégal;
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Département de Biologie Animale, Faculté des Sciences et Techniques, Université Cheikh Anta Diop de Dakar, Dakar Fann, Sénégal;
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Omar Thiaw
Omar Thiaw
Aix Marseille University, Institut de Recherche pour le Développement (IDR) (Dakar, Marseille, Papeete), AP-HM, Institut Hospitalo-Universitaire-Méditerranée Infection, UMR Vecteurs—Infections Tropicales et Méditerranéennes (VITROME), Marseille, France;
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Aurélie Cailleau
Aurélie Cailleau
Unité d’Entomologie Médicale (UME), Institut Pasteur Dakar, Dakar, Sénégal;
Centre Suisse de Recherches Scientifiques en Cote d’Ivoire (CSRS), Yopougon, Abidjan, Côte d’Ivoire;
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Centre Suisse de Recherches Scientifiques en Cote d’Ivoire (CSRS), Yopougon, Abidjan, Côte d’Ivoire;
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Nafissatou Diagne
Nafissatou Diagne
Aix Marseille University, Institut de Recherche pour le Développement (IDR) (Dakar, Marseille, Papeete), AP-HM, Institut Hospitalo-Universitaire-Méditerranée Infection, UMR Vecteurs—Infections Tropicales et Méditerranéennes (VITROME), Marseille, France;
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Myriam Harry
Myriam Harry
UMR Évolution, Génomes, Comportement, Écologie (EGCE) Centre National de la Recherche Scientifique (CNRS), IRD-University Paris-Sud, IDEEV, University Paris-Saclay, Gif-sur-Yvette Cedex, France
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Charles Bouganali
Charles Bouganali
Aix Marseille University, Institut de Recherche pour le Développement (IDR) (Dakar, Marseille, Papeete), AP-HM, Institut Hospitalo-Universitaire-Méditerranée Infection, UMR Vecteurs—Infections Tropicales et Méditerranéennes (VITROME), Marseille, France;
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Pape M. Sembène
Pape M. Sembène
Département de Biologie Animale, Faculté des Sciences et Techniques, Université Cheikh Anta Diop de Dakar, Dakar Fann, Sénégal;
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Souleymane Doucoure
Souleymane Doucoure
Aix Marseille University, Institut de Recherche pour le Développement (IDR) (Dakar, Marseille, Papeete), AP-HM, Institut Hospitalo-Universitaire-Méditerranée Infection, UMR Vecteurs—Infections Tropicales et Méditerranéennes (VITROME), Marseille, France;
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Cheikh Sokhna
Cheikh Sokhna
Aix Marseille University, Institut de Recherche pour le Développement (IDR) (Dakar, Marseille, Papeete), AP-HM, Institut Hospitalo-Universitaire-Méditerranée Infection, UMR Vecteurs—Infections Tropicales et Méditerranéennes (VITROME), Marseille, France;
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The implementation of long-lasting insecticidal-treated bed nets (LLINs) has contributed to halving the mortality rate due to malaria since 2000 in sub-Saharan Africa. These tools are highly effective against indoor-feeding malaria vectors. Thus, to achieve the World Health Assembly’s new target to reduce the burden of malaria over the next 15 years by 90%, it is necessary to understand how the spatiotemporal dynamics of malaria vectors and human exposure to bites is modified in the context of scaling up global efforts to control malaria transmission. This study was conducted in Dielmo, a Senegalese village, after the introduction of LLINs and two rounds of LLINs renewals. Data analysis showed that implementation of LLINs correlated with a significant decrease in the biting densities of the main malaria vectors, Anopheles gambiae s.l. and Anopheles funestus, reducing malaria transmission. Other environment factors likely contributed to the decrease in An. funestus, but this trend was enhanced with the introduction of LLINs. The bulk of bites occurred during sleeping hours, but the residual vector populations of An. gambiae s.l. and An. funestus had an increased propensity to bite outdoors, so a risk of infectious bites remained for LLINs users. These results highlight the need to increase the level and correct use of LLINs and to combine this intervention with complementary control measures against residual exposure, such as spatial repellents and larval source management, to achieve the goal of eliminating malaria transmission.
- Supplemental Materials (XLS 31 KB)
- Supplemental Materials (XLS 88 KB)
Author Notes
Financial support: This publication was made possible through support provided by the IDR-DPF (Institut de Recherche pour le Développement-Direction des Programmes de Recherche et de la Formation au Sud).
Authors’ addresses: Seynabou Sougoufara, Aix Marseille University, IRD (Dakar, Marseille, Papeete), AP-HM, IHU-Méditerranée Infection, UMR Vecteurs—Infections Tropicales et Méditerranéennes (VITROME), Marseille, France, and Département de Biologie Animale, Faculté des Sciences et Techniques, Université Cheikh Anta Diop de Dakar, Dakar Fann, Sénégal, E-mail: seynabou.sougoufara@gmail.com. Omar Thiaw, Nafissatou Diagne, Charles Bouganali, Souleymane Doucoure, and Cheikh Sokhna, Aix Marseille University, IRD (Dakar, Marseille, Papeete), AP-HM, IHU-Méditerranée Infection, UMR Vecteurs—Infections Tropicales et Méditerranéennes (VITROME), Marseille, France, E-mails: thiawomar185@yahoo.com, nafissatou.diagne@ird.fr, charles.bouganali@ird.fr, souleymane.doucoure@ird.fr, and cheikh.sokhna@ird.fr. Aurélie Cailleau, Unité d’Entomologie Médicale (UME), Institut Pasteur Dakar, Dakar, Sénégal, and Centre Suisse de Recherches Scientifiques en Cote d’Ivoire (CSRS), Yopougon, Abidjan, Côte d’Ivoire, E-mail: a.cailleau@csrs.ci. Myriam Harry, UMR Évolution, Génomes, Comportement, Écologie (EGCE) CNRS, IRD-University Paris-Sud, IDEEV, University Paris-Saclay, Gif-sur-Yvette Cedex, France, E-mail: myriam.harry@u-psud.fr. Pape M. Sembène, Département de Biologie Animale, Faculté des Sciences et Techniques, Université Cheikh Anta Diop de Dakar, Dakar Fann, Sénégal, E-mail: mbacke.sembene@ird.fr.
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
World Health Organization, 2015. World Malaria Report 2015. Geneva, Switzerland: WHO.
-
2.
Bayoh MN, Mathias DK, Odiere MR, Mutuku FM, Kamau L, Gimnig JE, Vulule JM, Hawley WA, Hamel MJ, Walker ED, 2010. Anopheles gambiae: historical population decline associated with regional distribution of insecticide-treated bed nets in western Nyanza Province, Kenya. Malar J 9: 62.
-
3.
Awolola ST, Adeogun AO, Olojede JB, Oduola AO, Oyewole IO, Amajoh CN, 2014. Impact of PermaNet 3.0 on entomological indices in an area of pyrethroid resistant Anopheles gambiae in south-western Nigeria. Parasit Vectors 7: 236.
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4.
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5.
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-
6.
Hetzel MW, Reimer LJ, Gideon G, Koimbu G, Barnadas C, Makita L, Siba PM, Mueller I, 2016. Changes in malaria burden and transmission in sentinel sites after the roll-out of long-lasting insecticidal nets in Papua New Guinea. Parasit Vectors 9: 340.
-
7.
Bhatt S et al. 2015. The effect of malaria control on Plasmodium falciparum in Africa between 2000 and 2015. Nature 526: 207–211.
-
8.
World Health Organization, 2015. Global Technical Strategy for Malaria 2016–2030. Geneva, Switzerland: WHO.
-
9.
Griffin JT et al. 2016. Potential for reduction of burden and local elimination of malaria by reducing Plasmodium falciparum malaria transmission: a mathematical modelling study. Lancet Infect Dis 16: 465–472.
-
10.
Trape JF et al. 2011. Malaria morbidity and pyrethroid resistance after the introduction of insecticide-treated bednets and artemisinin-based combination therapies: a longitudinal study. Lancet Infect Dis 11: 925–932.
-
11.
Zhou G, Afrane YA, Vardo-Zalik AM, Atieli H, Zhong D, Wamae P, Himeidan YE, Minakawa N, Githeko AK, Yan G, 2011. Changing patterns of malaria epidemiology between 2002 and 2010 in western Kenya: the fall and rise of malaria. PLoS One 6: e20318.
-
12.
Jagannathan P, Muhindo MK, Kakuru A, Arinaitwe E, Greenhouse B, Tappero J, Rosenthal PJ, Kaharuza F, Kamya MR, Dorsey G, 2012. Increasing incidence of malaria in children despite insecticide-treated bed nets and prompt anti-malarial therapy in Tororo, Uganda. Malar J 11: 435.
-
13.
Bayoh MN et al. 2014. Persistently high estimates of late night, indoor exposure to malaria vectors despite high coverage of insecticide treated nets. Parasit Vectors 7: 380.
-
14.
Ursing J, Rombo L, Rodrigues A, Aaby P, Kofoed PE, 2014. Malaria transmission in Bissau, Guinea-Bissau between 1995 and 2012: malaria resurgence did not negatively affect mortality. PLoS One 9: e0101167.
-
15.
Daniels RF et al. 2015. Modeling malaria genomics reveals transmission decline and rebound in Senegal. Proc Natl Acad Sci USA 112: 7067–7072.
-
16.
Ranson H, Lissenden N, 2016. Insecticide resistance in African Anopheles mosquitoes: a worsening situation that needs urgent action to maintain malaria control. Trends Parasitol 32: 187–196.
-
17.
Sougoufara S, Doucouré S, Sembène PM, Harry M, Sokhna C, 2017. Challenges for malaria vector control in sub-Saharan Africa: resistance and behavioral adaptations in Anopheles populations. J Vector Borne Dis 54: 4–15.
-
18.
Russell TL, Govella NJ, Azizi S, Drakeley CJ, Kachur SP, Killeen GF, 2011. Increased proportions of outdoor feeding among residual malaria vector populations following increased use of insecticide-treated nets in rural Tanzania. Malar J 10: 80.
-
19.
Reddy MR, Overgaard HJ, Abaga S, Reddy VP, Caccone A, Kiszewski AE, Slotman MA, 2011. Outdoor host seeking behaviour of Anopheles gambiae mosquitoes following initiation of malaria vector control on Bioko Island, Equatorial Guinea. Malar J 10: 184.
-
20.
Killeen GF, 2014. Characterizing, controlling and eliminating residual malaria transmission. Malar J 13: 330.
-
21.
Padonou GG, Gbedjissi G, Yadouleton A, Azondekon R, Razack O, Oussou O, Gnanguenon V, Rock A, Sezonlin M, Akogbeto M, 2012. Decreased proportions of indoor feeding and endophily in Anopheles gambiae s.l. populations following the indoor residual spraying and insecticide-treated net interventions in Benin (West Africa). Parasit Vectors 5: 262.
-
22.
Sougoufara S, Diédhiou SM, Doucouré S, Diagne N, Sembène PM, Harry M, Trape JF, Sokhna C, Ndiath MO, 2014. Biting by Anopheles funestus in broad daylight after use of long-lasting insecticidal nets: a new challenge to malaria elimination. Malar J 13: 125.
-
23.
Meyers JI et al. 2016. Increasing outdoor host-seeking in Anopheles gambiae over 6 years of vector control on Bioko Island. Malar J 15: 239.
-
24.
Sougoufara S, Harry M, Doucouré S, Sembène PM, Sokhna C, 2016. Shift in species composition in the Anopheles gambiae complex after implementation of long-lasting insecticidal nets in Dielmo, Senegal. Med Vet Entomol 30: 365–368.
-
25.
Scott TW, Takken W, 2012. Feeding strategies of anthropophilic mosquitoes result in increased risk of pathogen transmission. Trends Parasitol 28: 114–121.
-
26.
Trape JF et al. 1994. The Dielmo project: a longitudinal study of natural malaria infection and the mechanisms of protective immunity in a community living in a holoendemic area of Senegal. Am J Trop Med Hyg 51: 123–137.
-
27.
Trape JF et al. 2014. The rise and fall of malaria in a west African rural community, Dielmo, Senegal, from 1990 to 2012: a 22 year longitudinal study. Lancet Infect Dis 14: 476–488.
-
28.
Wotodjo AN, Diagne N, Gaudart J, Richard V, Raoult D, Sokhna C, 2015. Malaria risk factors in Dielmo, a Senegalese malaria-endemic village, between October and November of 2013: a case-control study. Am J Trop Med Hyg 92: 565–568.
-
29.
Gilles MT, De Meillon D, 1968. The anophelinae of Africa south of the Sahara. Publ South Afri Inst Med Res 54: 343.
-
30.
Wirtz RA, Duncan JF, Njelesani EK, Schneider I, Brown AE, Oster CN, Were JB, Webster HK, 1989. ELISA method for detecting Plasmodium falciparum circumsporozoite antibody. Bull World Health Organ 67: 535–542.
-
31.
Fournier DA, Skaug HJ, Ancheta J, Ianelli J, Magnusson A, Maunder MN, Nielsen A, Sibert J, 2012. AD model builder: using automatic differentiation for statistical inference of highly parameterized complex nonlinear models. Optim Methods Softw 27: 233–249.
-
32.
Skaug H, Fournier D, Magnusson A, Nielsen A, 2014. Generalized Linear Mixed Models Using AD Model Builder. (R Package v0.8.0). Available at: http://glmmadmb.r-forge.r-project.org/. Accessed August 20, 2017.
-
33.
The R Foundation, 2017. R: The R Project for Statistical Computing. Available at: https://www.r-project.org/. Accessed July 18, 2017.
-
34.
Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MHH, White J-SS, 2009. Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24: 127–135.
-
35.
Killeen GF, Kihonda J, Lyimo E, Oketch FR, Kotas ME, Mathenge E, Schellenberg JA, Lengeler C, Smith TA, Drakeley CJ, 2006. Quantifying behavioural interactions between humans and mosquitoes: evaluating the protective efficacy of insecticidal nets against malaria transmission in rural Tanzania. BMC Infect Dis 6: 161.
-
36.
Fontenille D, Lochouarn L, Diagne N, Sokhna C, Lemasson JJ, Diatta M, Konate L, Faye F, Rogier C, Trape JF, 1997. High annual and seasonal variations in malaria transmission by anophelines and vector species composition in Dielmo, a holoendemic area in Senegal. Am J Trop Med Hyg 56: 247–253.
-
37.
Faye O et al. 1995. La sécheresse et la baisse du paludisme dans les Niayes du Sénégal. Cah Détudes Rech Francoph Santé 5: 299–305.
-
38.
Mouchet J, Faye O, Julvez J, Manguin S, 1996. Drought and malaria retreat in the Sahel, west Africa. Lancet 348: 1735–1736.
-
39.
World Health Organization, 2011. Guidelines for Monitoring the Durability of Long-Lasting Insecticidal Mosquito Nets under Operational Conditions. Geneva, Switzerland: WHO.
-
40.
Wills AB et al. 2013. Physical durability of PermaNet 2.0 long-lasting insecticidal nets over three to 32 months of use in Ethiopia. Malar J 12: 242.
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