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Published in: Malaria Journal 1/2014

Open Access 01-12-2014 | Research

Entomological and parasitological impacts of indoor residual spraying with DDT, alphacypermethrin and deltamethrin in the western foothill area of Madagascar

Authors: Jocelyn Ratovonjato, Milijaona Randrianarivelojosia, Maroafy E Rakotondrainibe, Vaomalala Raharimanga, Lala Andrianaivolambo, Gilbert Le Goff, Christophe Rogier, Frédéric Ariey, Sébastien Boyer, Vincent Robert

Published in: Malaria Journal | Issue 1/2014

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Abstract

Background

In Madagascar, indoor residual spraying (IRS) with insecticide was part of the national malaria control programme since the middle of the twentieth century. It was mainly employed in the highlands and the foothill areas, which are prone to malaria epidemics. Prior to a policy change foreseeing a shift from DDT to pyrethroids, a study was carried out to assess the entomological and parasitological impacts of IRS in areas with DDT or pyrethroids and in areas without IRS.

Methods

The study was carried out from October 2002 to February 2005 in three communes of the western foothill area of Madagascar. Two communes received IRS with DDT in February 2003, then IRS with pyrethroids (alphacypermethrin or deltamethrin) in February 2004. The third commune remained untreated. Mosquitoes were collected at night using human landing catches and early in the morning in resting places. Blood smears were obtained from schoolchildren and microscopically examined for Plasmodium presence.

Results

In total, 18,168 human landing mosquitoes and 12,932 resting anophelines were collected. The Anopheles species caught comprised 10 species. The main and most abundant malaria vector was Anopheles funestus (72.3% of human-seeking malaria vectors caught indoors). After IRS had taken place, this species exhibited a lower human biting rate and a lower sporozoite index. Overall, 5,174 blood smears were examined with a mean plasmodic index of 19.9%. A total of four Plasmodium species were detected. Amongst tested school children the highest plasmodial index was 54.6% in the untreated commune, compared to 19.9% in the commune sprayed with DDT and 11.9% in the commune sprayed with pyrethroid. The highest prevalence of clinical malaria attacks in children present at school the day of the survey was 33% in the untreated commune compared to 8% in the areas which received IRS.

Conclusion

In terms of public health, the present study shows (1) a high efficacy of IRS with insecticide, (2) a similar efficacy of DDT and pyrethroid and (3) a similar efficacy of alphacypermethrin and deltamethrin. The use of IRS with DDT and pyrethroid greatly decreased the vector-human contact, with an associated decrease of the plasmodial index. However malaria transmission did not reach zero, probably due to the exophilic host-seeking and resting behaviours of the malaria vectors, thus avoiding contact with insecticide-treated surfaces indoors. The study highlights the strengths and weaknesses of the IRS implementation and the need for complementary tools for an optimal vector control in Madagascar.
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Literature
1.
go back to reference Randriantsimaniry D: Lutte antivectorielle dans l’épidémie de paludisme des plateaux de Madagascar. Santé. 1995, 6: 392-396. Randriantsimaniry D: Lutte antivectorielle dans l’épidémie de paludisme des plateaux de Madagascar. Santé. 1995, 6: 392-396.
2.
go back to reference Curtis CF, Mnzava AEP: Comparison of house spraying and insecticide treated nets for malaria control. Bull World Health Organ. 2000, 78: 1389-1400.PubMedCentralPubMed Curtis CF, Mnzava AEP: Comparison of house spraying and insecticide treated nets for malaria control. Bull World Health Organ. 2000, 78: 1389-1400.PubMedCentralPubMed
3.
go back to reference Lumaret R: Etude sur le paludisme à Madagascar, situation en 1962. 1963, Antananarivo: Service Antipaludique, Rapport dactylographié, 232- Lumaret R: Etude sur le paludisme à Madagascar, situation en 1962. 1963, Antananarivo: Service Antipaludique, Rapport dactylographié, 232-
4.
go back to reference Mouchet J, Carnevale P, Coosemans M, Julvez J, Manguin S, Richard-Lenoble D, Sircoulon J: Biodiversité du paludisme dans le monde. 2004, Montrouge: John Libbey Eurotext Mouchet J, Carnevale P, Coosemans M, Julvez J, Manguin S, Richard-Lenoble D, Sircoulon J: Biodiversité du paludisme dans le monde. 2004, Montrouge: John Libbey Eurotext
5.
go back to reference Fontenille D, Rakotoarivony I: Reappearance of Anopheles funestus as a malaria vector in the Antananarivo region, Madagascar. Trans R Soc Trop Med Hyg. 1988, 82: 644-645. 10.1016/0035-9203(88)90545-7.CrossRefPubMed Fontenille D, Rakotoarivony I: Reappearance of Anopheles funestus as a malaria vector in the Antananarivo region, Madagascar. Trans R Soc Trop Med Hyg. 1988, 82: 644-645. 10.1016/0035-9203(88)90545-7.CrossRefPubMed
6.
go back to reference Lepers JP, Fontenille D, Rason MD, Chougnet C, Astagneau P, Coulanges P, Deloron P: Transmission and epidemiology of newly transmitted falciparum malaria in the central highland plateaux of Madagascar. Ann Trop Med Parasitol. 1991, 85: 297-304.PubMed Lepers JP, Fontenille D, Rason MD, Chougnet C, Astagneau P, Coulanges P, Deloron P: Transmission and epidemiology of newly transmitted falciparum malaria in the central highland plateaux of Madagascar. Ann Trop Med Parasitol. 1991, 85: 297-304.PubMed
7.
go back to reference Rakotomanana F, Jeanne I, Duchemin J, Pietra V, Raharimalala L, Tombo M, Ariey F: Approche géographique dans la lutte contre le paludisme dans la région des Hautes Terres Centrales à Madagascar. Arch Inst Pasteur Madagascar. 2001, 67: 27-30.PubMed Rakotomanana F, Jeanne I, Duchemin J, Pietra V, Raharimalala L, Tombo M, Ariey F: Approche géographique dans la lutte contre le paludisme dans la région des Hautes Terres Centrales à Madagascar. Arch Inst Pasteur Madagascar. 2001, 67: 27-30.PubMed
8.
go back to reference Romi R, Razaiarimanga MC, Raharimanga R, Rakotondraibe EM, Ranaivo LH, Pietra V, Raveloson A, Majori G: Impact of the malaria control campaign (1993-1998) in the highlands of Madagascar: parasitological and entomological data. Am J Trop Med Hyg. 2002, 66: 75-82. Romi R, Razaiarimanga MC, Raharimanga R, Rakotondraibe EM, Ranaivo LH, Pietra V, Raveloson A, Majori G: Impact of the malaria control campaign (1993-1998) in the highlands of Madagascar: parasitological and entomological data. Am J Trop Med Hyg. 2002, 66: 75-82.
11.
go back to reference Sadasivaiah S, Tozan Y, Breman JG: Dichlorodiphenyltrichloroethane (DDT) for indoor residual spraying in Africa: how can it be used for malaria control?. Am J Trop Med Hyg. 2007, 77 (Suppl.6): 249-263.PubMed Sadasivaiah S, Tozan Y, Breman JG: Dichlorodiphenyltrichloroethane (DDT) for indoor residual spraying in Africa: how can it be used for malaria control?. Am J Trop Med Hyg. 2007, 77 (Suppl.6): 249-263.PubMed
12.
go back to reference Bouwman H, van den Berg H, Kylin H: DDT and malaria prevention: addressing the paradox. Environ Health Perspect. 2011, 119: 744-747. 10.1289/ehp.1002127.PubMedCentralCrossRefPubMed Bouwman H, van den Berg H, Kylin H: DDT and malaria prevention: addressing the paradox. Environ Health Perspect. 2011, 119: 744-747. 10.1289/ehp.1002127.PubMedCentralCrossRefPubMed
13.
go back to reference WHO: WHO/HTM/RBM/2004.54. Questions fréquemment posées à propos de l’utilisation du DDT pour la lutte antivectorielle. 2005, Geneva: World Health Organization WHO: WHO/HTM/RBM/2004.54. Questions fréquemment posées à propos de l’utilisation du DDT pour la lutte antivectorielle. 2005, Geneva: World Health Organization
14.
go back to reference Najera JA, Zaim M: Lutte contre les vecteurs du paludisme: Critères et procédures de prise de décision pour une utilisation raisonnée des insecticides. 2004, Geneva: World Health Organization, WHO_CDS_WHOPES_2002.5_Rev.1_Fre.pdf5 Najera JA, Zaim M: Lutte contre les vecteurs du paludisme: Critères et procédures de prise de décision pour une utilisation raisonnée des insecticides. 2004, Geneva: World Health Organization, WHO_CDS_WHOPES_2002.5_Rev.1_Fre.pdf5
15.
go back to reference Protopopoff N, Matowo J, Malima R, Kavishe R, Kaaya R, Wright A, West PA, Kleinschmidt I, Kisinza W, Mosha FW, Rowland M: High level of resistance in the mosquito Anopheles gambiae to pyrethroid insecticides and reduced susceptibility to bendiocarb in north-western Tanzania. Malar J. 2013, 12: 149-10.1186/1475-2875-12-149.PubMedCentralCrossRefPubMed Protopopoff N, Matowo J, Malima R, Kavishe R, Kaaya R, Wright A, West PA, Kleinschmidt I, Kisinza W, Mosha FW, Rowland M: High level of resistance in the mosquito Anopheles gambiae to pyrethroid insecticides and reduced susceptibility to bendiocarb in north-western Tanzania. Malar J. 2013, 12: 149-10.1186/1475-2875-12-149.PubMedCentralCrossRefPubMed
16.
go back to reference Chaccour CJ, Kobylinski KC, Bassat Q, Bousema T, Drakeley C, Alonso P, Foy BD: Ivermectin to reduce malaria transmission: a research agenda for a promising new tool for elimination. Malar J. 2013, 12: 153-10.1186/1475-2875-12-153.PubMedCentralCrossRefPubMed Chaccour CJ, Kobylinski KC, Bassat Q, Bousema T, Drakeley C, Alonso P, Foy BD: Ivermectin to reduce malaria transmission: a research agenda for a promising new tool for elimination. Malar J. 2013, 12: 153-10.1186/1475-2875-12-153.PubMedCentralCrossRefPubMed
17.
go back to reference Fuchs S, Nolan T, Crisanti A: Mosquito transgenic technologies to reduce Plasmodium transmission. Methods Mol Biol. 2013, 923: 601-622.CrossRefPubMed Fuchs S, Nolan T, Crisanti A: Mosquito transgenic technologies to reduce Plasmodium transmission. Methods Mol Biol. 2013, 923: 601-622.CrossRefPubMed
18.
go back to reference Carter R: Spatial simulation of malaria transmission and its control by malaria transmission blocking vaccination. Int J Parasitol. 2002, 32: 1617-1624. 10.1016/S0020-7519(02)00190-X.CrossRefPubMed Carter R: Spatial simulation of malaria transmission and its control by malaria transmission blocking vaccination. Int J Parasitol. 2002, 32: 1617-1624. 10.1016/S0020-7519(02)00190-X.CrossRefPubMed
19.
go back to reference Padonou GG, Gbedjissi G, Yadouleton A, Azondekon R, Razack O, Oussou O, Gnanguenon V, Rock A, Sezonlin M, Akogbeto M: 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. 2012, 5: 262-10.1186/1756-3305-5-262.PubMedCentralCrossRefPubMed Padonou GG, Gbedjissi G, Yadouleton A, Azondekon R, Razack O, Oussou O, Gnanguenon V, Rock A, Sezonlin M, Akogbeto M: 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. 2012, 5: 262-10.1186/1756-3305-5-262.PubMedCentralCrossRefPubMed
20.
go back to reference Sharp BL, Ridl FC, Govender D, Kuklinski J, Kleinschmidt I: Malaria vector control by indoor residual insecticide spraying on the tropical island of Bioko: Equatorial Guinea. Malar J. 2007, 6: 52-10.1186/1475-2875-6-52.PubMedCentralCrossRefPubMed Sharp BL, Ridl FC, Govender D, Kuklinski J, Kleinschmidt I: Malaria vector control by indoor residual insecticide spraying on the tropical island of Bioko: Equatorial Guinea. Malar J. 2007, 6: 52-10.1186/1475-2875-6-52.PubMedCentralCrossRefPubMed
21.
go back to reference Robert V, Groupe de Recherche sur le Paludisme: Evaluation des insecticides de remplacement du DDT dans les CAID (Campagnes d’Aspersion Intra-Domiciliaire d’insecticide) sur les Hautes Terres Centrales de Madagascar—Premier rapport comparant un traitement DDT à un témoin négatif dans le Moyen-Ouest (zone de Mahasolo) entre octobre 2002 et septembre 2003. 2003, Antananarivo: Institut Pasteur de Madagascar, 62-002DocTech-IPM/2003 Robert V, Groupe de Recherche sur le Paludisme: Evaluation des insecticides de remplacement du DDT dans les CAID (Campagnes d’Aspersion Intra-Domiciliaire d’insecticide) sur les Hautes Terres Centrales de Madagascar—Premier rapport comparant un traitement DDT à un témoin négatif dans le Moyen-Ouest (zone de Mahasolo) entre octobre 2002 et septembre 2003. 2003, Antananarivo: Institut Pasteur de Madagascar, 62-002DocTech-IPM/2003
22.
go back to reference Robert V, Groupe de Recherche sur le Paludisme: Evaluation des insecticides de remplacement du DDT dans les CAID (Campagnes d’Aspersion Intra-Domiciliaire d’insecticide) sur les Hautes Terres Centrales de Madagascar—Deuxième rapport comparant un traitement à l’alphacyperméthrine ou à la deltaméthrine à un témoin négatif dans le Moyen-Ouest (zone de Mahasolo) entre octobre 2003 et septembre 2004. 2005, Antananarivo: Institut Pasteur de Madagascar, 71-002DocTech-IPM/Entomo/2005 Robert V, Groupe de Recherche sur le Paludisme: Evaluation des insecticides de remplacement du DDT dans les CAID (Campagnes d’Aspersion Intra-Domiciliaire d’insecticide) sur les Hautes Terres Centrales de Madagascar—Deuxième rapport comparant un traitement à l’alphacyperméthrine ou à la deltaméthrine à un témoin négatif dans le Moyen-Ouest (zone de Mahasolo) entre octobre 2003 et septembre 2004. 2005, Antananarivo: Institut Pasteur de Madagascar, 71-002DocTech-IPM/Entomo/2005
23.
go back to reference Ratovonjato J, Rakotoson R: Evaluation de la rémanence des deux pyréthinoïdes: l’alphacyperméthrine 5% et la deltaméthrine WG 250 de novembre 2004 à février 2005 dans le district de Tsiroanomandidy, Madagascar. 2007, Antananarivo: Institut Pasteur de Madagascar, 27-002DocTech-IPM/2007 Ratovonjato J, Rakotoson R: Evaluation de la rémanence des deux pyréthinoïdes: l’alphacyperméthrine 5% et la deltaméthrine WG 250 de novembre 2004 à février 2005 dans le district de Tsiroanomandidy, Madagascar. 2007, Antananarivo: Institut Pasteur de Madagascar, 27-002DocTech-IPM/2007
24.
go back to reference Robert V, Le Goff G, Andrianaivolambo L, Randimby FM, Domarle O, Randrianarivelojosia M, Raharimanga V, Raveloson A, Ravaonjanahary C, Ariey F: Moderate transmission but high prevalence of malaria in Madagascar. Int J Parasitol. 2006, 36: 1273-1281. 10.1016/j.ijpara.2006.06.005.CrossRefPubMed Robert V, Le Goff G, Andrianaivolambo L, Randimby FM, Domarle O, Randrianarivelojosia M, Raharimanga V, Raveloson A, Ravaonjanahary C, Ariey F: Moderate transmission but high prevalence of malaria in Madagascar. Int J Parasitol. 2006, 36: 1273-1281. 10.1016/j.ijpara.2006.06.005.CrossRefPubMed
25.
go back to reference Grejbine A: Insectes Diptères Culicidae Anophelinae. Faune de Madagascar. 1966, 22: Paris, ORSTOM CNRS Grejbine A: Insectes Diptères Culicidae Anophelinae. Faune de Madagascar. 1966, 22: Paris, ORSTOM CNRS
26.
go back to reference Brutus L, Le Goff G, Rasoloniaina LG, Rajaonarivelo V, Raveloson A, Cot M: Lutte contre le paludisme dans le Moyen-Ouest de Madagascar: comparaison de l’efficacité de la lambda-cyhalothrin et du DDT en aspersions intra-domiciliaires: II–Etude entomologique. Parasite. 2001, 8: 297-308.CrossRefPubMed Brutus L, Le Goff G, Rasoloniaina LG, Rajaonarivelo V, Raveloson A, Cot M: Lutte contre le paludisme dans le Moyen-Ouest de Madagascar: comparaison de l’efficacité de la lambda-cyhalothrin et du DDT en aspersions intra-domiciliaires: II–Etude entomologique. Parasite. 2001, 8: 297-308.CrossRefPubMed
27.
go back to reference Le Goff G, Randimby FM, Rajaonarivelo V, Laganier R, Leong Pock Tsy JM, Ceianu CS, Duchemin JB, Robert R: Anopheles mascarensis de Meillon 1947, vecteur de paludisme dans le Moyen-Ouest de Madagascar?. Arch Inst Pasteur Madagascar. 2003, 69: 57-62.PubMed Le Goff G, Randimby FM, Rajaonarivelo V, Laganier R, Leong Pock Tsy JM, Ceianu CS, Duchemin JB, Robert R: Anopheles mascarensis de Meillon 1947, vecteur de paludisme dans le Moyen-Ouest de Madagascar?. Arch Inst Pasteur Madagascar. 2003, 69: 57-62.PubMed
28.
go back to reference Rajaonarivelo V, Le Goff G, Cot M, Brutus L: Les anophèles et la transmission du paludisme à Ambohimena, village de la marge occidentale des Hautes-Terres de Madagascar. Parasite. 2004, 11: 75-82.CrossRefPubMed Rajaonarivelo V, Le Goff G, Cot M, Brutus L: Les anophèles et la transmission du paludisme à Ambohimena, village de la marge occidentale des Hautes-Terres de Madagascar. Parasite. 2004, 11: 75-82.CrossRefPubMed
29.
go back to reference Fontenille D, Lepers JP, Campbell GH, Coluzzi M, Rakotoarivony I, Coulanges P: Malaria transmission and vector biology in Manarintsoa, high plateaux of Madagascar. Am J Trop Med Hyg. 1990, 43: 107-115.PubMed Fontenille D, Lepers JP, Campbell GH, Coluzzi M, Rakotoarivony I, Coulanges P: Malaria transmission and vector biology in Manarintsoa, high plateaux of Madagascar. Am J Trop Med Hyg. 1990, 43: 107-115.PubMed
30.
go back to reference Gillies MT, Coetzeee MC: A supplement to the Anophelinae of Africa south of the Sahara (Afrotropical region). 1987, Johannesburg: The South African Institute for Medical Research, 143-n°55 Gillies MT, Coetzeee MC: A supplement to the Anophelinae of Africa south of the Sahara (Afrotropical region). 1987, Johannesburg: The South African Institute for Medical Research, 143-n°55
31.
go back to reference Duchemin JB, Leong Pock Tsy JM, Rabarison P, Roux J, Coluzzi M, Costantini C: Zoophily of Anopheles arabiensis and A. gambiae in Madagascar demonstrated by odour-baited entry traps. Med Vet Entomol. 2001, 15: 50-57. 10.1046/j.1365-2915.2001.00276.x.CrossRefPubMed Duchemin JB, Leong Pock Tsy JM, Rabarison P, Roux J, Coluzzi M, Costantini C: Zoophily of Anopheles arabiensis and A. gambiae in Madagascar demonstrated by odour-baited entry traps. Med Vet Entomol. 2001, 15: 50-57. 10.1046/j.1365-2915.2001.00276.x.CrossRefPubMed
32.
go back to reference Albonico M, De Giorgi F, Razanakolona J, Raveloson A, Sabatinelli G, Pietra V, Modiano D: Control of epidemic malaria in the highlands of Madagascar. Parassitologia. 1999, 41: 373-376.PubMed Albonico M, De Giorgi F, Razanakolona J, Raveloson A, Sabatinelli G, Pietra V, Modiano D: Control of epidemic malaria in the highlands of Madagascar. Parassitologia. 1999, 41: 373-376.PubMed
33.
go back to reference Cot M, Brutus L, Le Goff G, Rajaonarivelo V, Raveloson A: Lutte contre le paludisme dans le Moyen-Ouest de Madagascar: comparaison de l’efficacité de la lambda-cyhalothrin et du DDT en aspersions intra-domiciliaires: II–Etude parasitologique et clinique. Parasite. 2001, 8: 309-316.CrossRefPubMed Cot M, Brutus L, Le Goff G, Rajaonarivelo V, Raveloson A: Lutte contre le paludisme dans le Moyen-Ouest de Madagascar: comparaison de l’efficacité de la lambda-cyhalothrin et du DDT en aspersions intra-domiciliaires: II–Etude parasitologique et clinique. Parasite. 2001, 8: 309-316.CrossRefPubMed
34.
go back to reference Jambou R, Ranaivo L, Raharimalala L, Randrianaivo J, Rakotomanana F, Modiano D, Pietra V, Boisier P, Rabarijaona L, Rabe T, Raveloson N, de Giorgi F: Malaria in the highlands of Madagascar after five years of indoor house spraying of DDT. Trans R Soc Trop Med Hyg. 2001, 95: 14-18. 10.1016/S0035-9203(01)90317-7.CrossRefPubMed Jambou R, Ranaivo L, Raharimalala L, Randrianaivo J, Rakotomanana F, Modiano D, Pietra V, Boisier P, Rabarijaona L, Rabe T, Raveloson N, de Giorgi F: Malaria in the highlands of Madagascar after five years of indoor house spraying of DDT. Trans R Soc Trop Med Hyg. 2001, 95: 14-18. 10.1016/S0035-9203(01)90317-7.CrossRefPubMed
35.
go back to reference WHO: Entomological field techniques for malaria control. 1992, Geneva: World Health Organization WHO: Entomological field techniques for malaria control. 1992, Geneva: World Health Organization
36.
go back to reference Muirhead-Thomson RC: A pit shelter for sampling outdoor mosquito population. Bull World Health Organ. 1958, 19: 241-261. Muirhead-Thomson RC: A pit shelter for sampling outdoor mosquito population. Bull World Health Organ. 1958, 19: 241-261.
37.
go back to reference Scott JA, Brogdon WG, Collins FH: Identification of single specimens of the Anopheles gambiae complex by the polymerase chain réaction. Am J Trop Med Hyg. 1993, 12: 520-529. Scott JA, Brogdon WG, Collins FH: Identification of single specimens of the Anopheles gambiae complex by the polymerase chain réaction. Am J Trop Med Hyg. 1993, 12: 520-529.
38.
go back to reference Léong Pock Tsy JM, Duchemin JB, Marrama L, Rabarison P, Le Goff G, Rajaonarivelo V, Robert V: Distribution of the species of the Anopheles gambiae complex, and first evidences of Anopheles merus as malaria vector in Madagascar. Malar J. 2003, 2: 33-10.1186/1475-2875-2-33.CrossRef Léong Pock Tsy JM, Duchemin JB, Marrama L, Rabarison P, Le Goff G, Rajaonarivelo V, Robert V: Distribution of the species of the Anopheles gambiae complex, and first evidences of Anopheles merus as malaria vector in Madagascar. Malar J. 2003, 2: 33-10.1186/1475-2875-2-33.CrossRef
39.
go back to reference Detinova TS: Age-grouping methods in Diptera of medical importance with special reference to some vectors of malaria. Monogr Ser World Health Organ. 1962, 47: 13-191.PubMed Detinova TS: Age-grouping methods in Diptera of medical importance with special reference to some vectors of malaria. Monogr Ser World Health Organ. 1962, 47: 13-191.PubMed
40.
go back to reference Beier JC, Perkins PV, Wirtz RA, Koros J, Diggs D, Gargan TP, Koech DK: Bloodmeal identification by direct-enzyme linked immunosorbent assay (ELISA), tested on Anopheles (Diptera: Culicidae) in Kenya. J Med Entomol. 1988, 25: 9-16.CrossRefPubMed Beier JC, Perkins PV, Wirtz RA, Koros J, Diggs D, Gargan TP, Koech DK: Bloodmeal identification by direct-enzyme linked immunosorbent assay (ELISA), tested on Anopheles (Diptera: Culicidae) in Kenya. J Med Entomol. 1988, 25: 9-16.CrossRefPubMed
41.
go back to reference Wirtz RA, Zavala F, Charoenvit Y, Campbell GH, Burkott TR, Schneir I, Esser KM, Beaudoin RL, André RG: Comparative testing of monoclonal antibodies against Plasmodium falciparum sporozoites for ELISA development. Bull World Health Organ. 1987, 65: 39-45.PubMedCentralPubMed Wirtz RA, Zavala F, Charoenvit Y, Campbell GH, Burkott TR, Schneir I, Esser KM, Beaudoin RL, André RG: Comparative testing of monoclonal antibodies against Plasmodium falciparum sporozoites for ELISA development. Bull World Health Organ. 1987, 65: 39-45.PubMedCentralPubMed
42.
go back to reference Andrianaivolambo L, Domarle O, Randrianarivelojosia M, Ratovonjato J, Le Goff G, Talman A, Ariey F, Robert V: Anthropophilic mosquitoes and malaria transmission in the eastern foothills of the central highlands of Madagascar. Acta Trop. 2010, 116: 240-245. 10.1016/j.actatropica.2010.08.017.CrossRefPubMed Andrianaivolambo L, Domarle O, Randrianarivelojosia M, Ratovonjato J, Le Goff G, Talman A, Ariey F, Robert V: Anthropophilic mosquitoes and malaria transmission in the eastern foothills of the central highlands of Madagascar. Acta Trop. 2010, 116: 240-245. 10.1016/j.actatropica.2010.08.017.CrossRefPubMed
43.
go back to reference WHO: Terminology of malaria and malaria eradication: technical report. 1963, Geneva: World Health Organization WHO: Terminology of malaria and malaria eradication: technical report. 1963, Geneva: World Health Organization
44.
go back to reference Basseri H, Raeisi A, Khakha MR, Pakarai A, Abdolghafar H: Seasonal abundance and host-feeding patterns of anopheline vectors in malaria endemic area of Iran. J Parasitol Res. 2010, 2010: 671291-PubMedCentralCrossRefPubMed Basseri H, Raeisi A, Khakha MR, Pakarai A, Abdolghafar H: Seasonal abundance and host-feeding patterns of anopheline vectors in malaria endemic area of Iran. J Parasitol Res. 2010, 2010: 671291-PubMedCentralCrossRefPubMed
45.
go back to reference Pappa V, Reddy M, Overgaard HJ, Abaga S, Caccone A: Estimation of the human blood index in malaria mosquito vectors in Equatorial Guinea after indoor antivector interventions. Am J Trop Med Hyg. 2011, 84: 298-301. 10.4269/ajtmh.2011.10-0463.PubMedCentralCrossRefPubMed Pappa V, Reddy M, Overgaard HJ, Abaga S, Caccone A: Estimation of the human blood index in malaria mosquito vectors in Equatorial Guinea after indoor antivector interventions. Am J Trop Med Hyg. 2011, 84: 298-301. 10.4269/ajtmh.2011.10-0463.PubMedCentralCrossRefPubMed
46.
go back to reference Gruchet H: Etude de l’âge physiologique des femelles d’Anopheles funestus funestus Giles dans la région de Miandrivazo, Madagascar. Bull Soc Path Exot. 1962, 55: 165-174.PubMed Gruchet H: Etude de l’âge physiologique des femelles d’Anopheles funestus funestus Giles dans la région de Miandrivazo, Madagascar. Bull Soc Path Exot. 1962, 55: 165-174.PubMed
47.
go back to reference Boisier P, Jambou R, Raharimalala L, Roux J: Relation between parasite density and fever risk in a community exposed to low level of malaria transmission in Madagascar highlands. Am J Trop Med Hyg. 2002, 67: 137-140.PubMed Boisier P, Jambou R, Raharimalala L, Roux J: Relation between parasite density and fever risk in a community exposed to low level of malaria transmission in Madagascar highlands. Am J Trop Med Hyg. 2002, 67: 137-140.PubMed
48.
go back to reference Taufflieb R, Saugrain J: Anophélisme sans paludisme au Nord du Tchad. Bull Soc Pathol Exot. 1960, 2: 150-152. Taufflieb R, Saugrain J: Anophélisme sans paludisme au Nord du Tchad. Bull Soc Pathol Exot. 1960, 2: 150-152.
49.
go back to reference Groupe de Recherche sur le Paludisme: Atlas évolutif du paludisme à Madagascar. 2002, Antananarivo: Institut Pasteur de Madagascar, 33- Groupe de Recherche sur le Paludisme: Atlas évolutif du paludisme à Madagascar. 2002, Antananarivo: Institut Pasteur de Madagascar, 33-
50.
go back to reference Githeko AK, Adungo NI, Karanja DM, Hawley WA, Vulule JM, Seroney IK, Ofulla AV, Atieli FK, Ondijo SO, Genga IO, Odada PK, Situbi PA, Oloo JA: Some observations on the biting behavior of Anopheles gambiae s.s., Anopheles arabiensis and Anopheles funestus and their implications for malaria control. Exp Parasitol. 1996, 82: 306-315. 10.1006/expr.1996.0038.CrossRefPubMed Githeko AK, Adungo NI, Karanja DM, Hawley WA, Vulule JM, Seroney IK, Ofulla AV, Atieli FK, Ondijo SO, Genga IO, Odada PK, Situbi PA, Oloo JA: Some observations on the biting behavior of Anopheles gambiae s.s., Anopheles arabiensis and Anopheles funestus and their implications for malaria control. Exp Parasitol. 1996, 82: 306-315. 10.1006/expr.1996.0038.CrossRefPubMed
51.
go back to reference Tirados I, Costantini C, Gibson G, Torr SJ: Blood-feeding behaviour of the malarial mosquito Anopheles arabiensis: implications for vector control. Med Vet Entomol. 2006, 20: 425-437. 10.1111/j.1365-2915.2006.652.x.CrossRefPubMed Tirados I, Costantini C, Gibson G, Torr SJ: Blood-feeding behaviour of the malarial mosquito Anopheles arabiensis: implications for vector control. Med Vet Entomol. 2006, 20: 425-437. 10.1111/j.1365-2915.2006.652.x.CrossRefPubMed
52.
go back to reference Durnez L, Van Bortel W, Denis L, Roelants P, Veracx A, Trung HD, Sochantha T, Coosemans M: False positive circumsporozoite protein ELISA: a challenge for the estimation of the entomological inoculation rate of malaria and for vector incrimination. Malar J. 2011, 10: 195-10.1186/1475-2875-10-195.PubMedCentralCrossRefPubMed Durnez L, Van Bortel W, Denis L, Roelants P, Veracx A, Trung HD, Sochantha T, Coosemans M: False positive circumsporozoite protein ELISA: a challenge for the estimation of the entomological inoculation rate of malaria and for vector incrimination. Malar J. 2011, 10: 195-10.1186/1475-2875-10-195.PubMedCentralCrossRefPubMed
53.
go back to reference Fontenille D, Meunier JY, Nkondjio CA, Tchuinkam T: Use of circumsporozoite protein enzyme-linked immunosorbent assay compared with microscopic examination of salivary glands for calculation of malaria infectivity rates in mosquitoes (Diptera: Culicidae) from Cameroon. J Med Entomol. 2001, 38: 451-454. 10.1603/0022-2585-38.3.451.CrossRefPubMed Fontenille D, Meunier JY, Nkondjio CA, Tchuinkam T: Use of circumsporozoite protein enzyme-linked immunosorbent assay compared with microscopic examination of salivary glands for calculation of malaria infectivity rates in mosquitoes (Diptera: Culicidae) from Cameroon. J Med Entomol. 2001, 38: 451-454. 10.1603/0022-2585-38.3.451.CrossRefPubMed
54.
go back to reference Lochouarn L, Fontenille D: ELISA detection of malaria sporozoites: false-positive results in Anopheles gambiae s.l. associated with bovine bloodmeals. Trans R Soc Trop Med Hyg. 1999, 93: 101-102. 10.1016/S0035-9203(99)90198-0.CrossRefPubMed Lochouarn L, Fontenille D: ELISA detection of malaria sporozoites: false-positive results in Anopheles gambiae s.l. associated with bovine bloodmeals. Trans R Soc Trop Med Hyg. 1999, 93: 101-102. 10.1016/S0035-9203(99)90198-0.CrossRefPubMed
55.
go back to reference Ayala D, Le Goff G, Robert V, De Jong P, Takken W: Population structure of the malaria vector Anopheles funestus (Diptera: Culicidae) in Madagascar and Comoros. Acta Trop. 2006, 97: 292-300. 10.1016/j.actatropica.2005.12.002.CrossRefPubMed Ayala D, Le Goff G, Robert V, De Jong P, Takken W: Population structure of the malaria vector Anopheles funestus (Diptera: Culicidae) in Madagascar and Comoros. Acta Trop. 2006, 97: 292-300. 10.1016/j.actatropica.2005.12.002.CrossRefPubMed
56.
go back to reference Randrianarivelojosia M, Raveloson A, Randriamanantena A, Juliano JJ, Andrianjafy T, Raharimalala LA, Robert V: Lessons learnt from the six decades of chloroquine use (1945-2005) to control malaria in Madagascar. Trans R Soc Trop Med Hyg. 2009, 103: 3-10. 10.1016/j.trstmh.2008.09.013.CrossRefPubMed Randrianarivelojosia M, Raveloson A, Randriamanantena A, Juliano JJ, Andrianjafy T, Raharimalala LA, Robert V: Lessons learnt from the six decades of chloroquine use (1945-2005) to control malaria in Madagascar. Trans R Soc Trop Med Hyg. 2009, 103: 3-10. 10.1016/j.trstmh.2008.09.013.CrossRefPubMed
Metadata
Title
Entomological and parasitological impacts of indoor residual spraying with DDT, alphacypermethrin and deltamethrin in the western foothill area of Madagascar
Authors
Jocelyn Ratovonjato
Milijaona Randrianarivelojosia
Maroafy E Rakotondrainibe
Vaomalala Raharimanga
Lala Andrianaivolambo
Gilbert Le Goff
Christophe Rogier
Frédéric Ariey
Sébastien Boyer
Vincent Robert
Publication date
01-12-2014
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2014
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/1475-2875-13-21

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