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Published in: Malaria Journal 1/2016

Open Access 01-12-2016 | Research

Does insecticide resistance contribute to heterogeneities in malaria transmission in The Gambia?

Authors: Kevin Ochieng’ Opondo, David Weetman, Musa Jawara, Mathurin Diatta, Amfaal Fofana, Florence Crombe, Julia Mwesigwa, Umberto D’Alessandro, Martin James Donnelly

Published in: Malaria Journal | Issue 1/2016

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Abstract

Background

Malaria hotspots, areas with consistently higher than average transmission, may become increasingly common as malaria declines. This phenomenon, currently observed in The Gambia, may be caused by several factors, including some related to the local vectors, whose contribution is poorly understood.

Methods

Using WHO susceptibility bioassays, insecticide resistance status was determined in vector populations sampled from six pairs of villages across The Gambia, each pair contained a low and high prevalence village.

Results

Three vector species were observed (23.5 % Anopheles arabiensis, 31.2 % Anopheles gambiae, 43.3 % Anopheles coluzzii and 2.0 % An. coluzzii × An. gambiae hybrids). Even at a fine scale, significant differences in species composition were detected within village pairs. Resistance to both DDT and deltamethrin was more common in An. gambiae, most markedly in the eastern part of The Gambia and partly attributable to differing frequencies of resistance mutations. The Vgsc-1014F target site mutation was strongly associated with both DDT (OR = 256.7, (95 % CI 48.6–6374.3, p < 0.001) and deltamethrin survival (OR = 9.14, (95 % CI 4.24–21.4, p < 0.001). A second target site mutation, Vgsc-1575Y, which co-occurs with Vgsc-1014F, and a metabolic marker of resistance, Gste2-114T, conferred additional survival benefits to both insecticides. DDT resistance occurred significantly more frequently in villages with high malaria prevalence (p = 0.025) though this did not apply to deltamethrin resistance.

Conclusion

Whilst causality of relationships requires further investigation, variation in vector species and insecticide resistance in The Gambia is associated with malaria endemicity; with a notably higher prevalence of infection and insecticide resistance in the east of the country. In areas with heterogeneous malaria transmission, the role of the vector should be investigated to guide malaria control interventions.
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Literature
1.
go back to reference Gaudart J, Poudiougou B, Dicko A, Ranque S, Toure O, Sagara I, et al. Space-time clustering of childhood malaria at the household level: a dynamic cohort in a Mali village. BMC Public Health. 2006;6:286.CrossRefPubMedPubMedCentral Gaudart J, Poudiougou B, Dicko A, Ranque S, Toure O, Sagara I, et al. Space-time clustering of childhood malaria at the household level: a dynamic cohort in a Mali village. BMC Public Health. 2006;6:286.CrossRefPubMedPubMedCentral
2.
go back to reference Ernst KC, Adoka SO, Kowuor DO, Wilson ML, John CC. Malaria hotspot areas in a highland Kenya site are consistent in epidemic and non-epidemic years and are associated with ecological factors. Malar J. 2006;5:78.CrossRefPubMedPubMedCentral Ernst KC, Adoka SO, Kowuor DO, Wilson ML, John CC. Malaria hotspot areas in a highland Kenya site are consistent in epidemic and non-epidemic years and are associated with ecological factors. Malar J. 2006;5:78.CrossRefPubMedPubMedCentral
3.
go back to reference Kreuels B, Kobbe R, Adjei S, Kreuzberg C, von Reden C, Bäter K, et al. Spatial variation of malaria incidence in young children from a geographically homogeneous area with high endemicity. J Infect Dis. 2008;197:85–93.CrossRefPubMed Kreuels B, Kobbe R, Adjei S, Kreuzberg C, von Reden C, Bäter K, et al. Spatial variation of malaria incidence in young children from a geographically homogeneous area with high endemicity. J Infect Dis. 2008;197:85–93.CrossRefPubMed
4.
go back to reference Bejon P, Williams TN, Liljander A, Noor AM, Wambua J, Ogada E, et al. Stable and unstable malaria hotspots in longitudinal cohort studies in Kenya. PLoS Med. 2010;7:e1000304.CrossRefPubMedPubMedCentral Bejon P, Williams TN, Liljander A, Noor AM, Wambua J, Ogada E, et al. Stable and unstable malaria hotspots in longitudinal cohort studies in Kenya. PLoS Med. 2010;7:e1000304.CrossRefPubMedPubMedCentral
5.
go back to reference Macdonald G. The analysis of malaria epidemics. Trop Dis Bull. 1953;50:871.PubMed Macdonald G. The analysis of malaria epidemics. Trop Dis Bull. 1953;50:871.PubMed
6.
go back to reference WHO. World Malaria Report 2013. Geneva: World Health Organization. 2013. WHO. World Malaria Report 2013. Geneva: World Health Organization. 2013.
7.
go back to reference WHO. Malaria elimination: a field manual for low and moderate endemic countries. Geneva: World Health Organization. 2007. WHO. Malaria elimination: a field manual for low and moderate endemic countries. Geneva: World Health Organization. 2007.
8.
go back to reference Woolhouse ME, Dye C, Etard J-F, Smith T, Charlwood J, Garnett G, et al. Heterogeneities in the transmission of infectious agents: implications for the design of control programs. Proc Natl Acad Sci USA. 1997;94:338–42.CrossRefPubMedPubMedCentral Woolhouse ME, Dye C, Etard J-F, Smith T, Charlwood J, Garnett G, et al. Heterogeneities in the transmission of infectious agents: implications for the design of control programs. Proc Natl Acad Sci USA. 1997;94:338–42.CrossRefPubMedPubMedCentral
9.
go back to reference Bousema T, Drakeley C, Gesase S, Hashim R, Magesa S, Mosha F, et al. Identification of hot spots of malaria transmission for targeted malaria control. J Infect Dis. 2010;201:1764–74.CrossRefPubMed Bousema T, Drakeley C, Gesase S, Hashim R, Magesa S, Mosha F, et al. Identification of hot spots of malaria transmission for targeted malaria control. J Infect Dis. 2010;201:1764–74.CrossRefPubMed
10.
go back to reference Thomas C, Lindsay S. Local-scale variation in malaria infection amongst rural Gambian children estimated by satellite remote sensing. Trans R Soc Trop Med Hyg. 2000;94:159–63.CrossRefPubMed Thomas C, Lindsay S. Local-scale variation in malaria infection amongst rural Gambian children estimated by satellite remote sensing. Trans R Soc Trop Med Hyg. 2000;94:159–63.CrossRefPubMed
11.
go back to reference Burkot TR, Graves PM, Paru R, Wirtz RA, Heywood PF. Human malaria transmission studies in the Anopheles punctulatus complex in Papua New Guinea: sporozoite rates, inoculation rates, and sporozoite densities. Am J Trop Med Hyg. 1988;39:135–44.PubMed Burkot TR, Graves PM, Paru R, Wirtz RA, Heywood PF. Human malaria transmission studies in the Anopheles punctulatus complex in Papua New Guinea: sporozoite rates, inoculation rates, and sporozoite densities. Am J Trop Med Hyg. 1988;39:135–44.PubMed
12.
go back to reference Browne E, Frimpong E, Sievertsen J, Hagen J, Hamelmann C, Dietz K, et al. Malariometric update for the rainforest and savanna of Ashanti region. Ghana. Ann Trop Med Parasitol. 2000;94:15–22.CrossRefPubMed Browne E, Frimpong E, Sievertsen J, Hagen J, Hamelmann C, Dietz K, et al. Malariometric update for the rainforest and savanna of Ashanti region. Ghana. Ann Trop Med Parasitol. 2000;94:15–22.CrossRefPubMed
13.
go back to reference Mwesigwa J, Okebe J, Affara M, Di Tanna GL, Nwakanma D, Janha O, et al. On-going malaria transmission in The Gambia despite high coverage of control interventions: a nationwide cross-sectional survey. Malar J. 2015;14:314.CrossRefPubMedPubMedCentral Mwesigwa J, Okebe J, Affara M, Di Tanna GL, Nwakanma D, Janha O, et al. On-going malaria transmission in The Gambia despite high coverage of control interventions: a nationwide cross-sectional survey. Malar J. 2015;14:314.CrossRefPubMedPubMedCentral
14.
go back to reference GNMCP. Malaria Indicator Survey. Banjul: National Malaria Control Programme. 2011. GNMCP. Malaria Indicator Survey. Banjul: National Malaria Control Programme. 2011.
15.
go back to reference Stoddard ST, Morrison AC, Vazquez-Prokopec GM, Soldan VP, Kochel TJ, Kitron U, et al. The role of human movement in the transmission of vector-borne pathogens. PLoS Negl Trop Dis. 2009;3:e481.CrossRefPubMedPubMedCentral Stoddard ST, Morrison AC, Vazquez-Prokopec GM, Soldan VP, Kochel TJ, Kitron U, et al. The role of human movement in the transmission of vector-borne pathogens. PLoS Negl Trop Dis. 2009;3:e481.CrossRefPubMedPubMedCentral
16.
go back to reference Klinkenberg E, McCall P, Wilson MD, Akoto AO, Amerasinghe FP, Bates I, et al. Urban malaria and anaemia in children: a cross-sectional survey in two cities of Ghana. Trop Med Int Health. 2006;11:578–88.CrossRefPubMed Klinkenberg E, McCall P, Wilson MD, Akoto AO, Amerasinghe FP, Bates I, et al. Urban malaria and anaemia in children: a cross-sectional survey in two cities of Ghana. Trop Med Int Health. 2006;11:578–88.CrossRefPubMed
17.
18.
go back to reference Smith T, Charlwood J, Takken W, Tanner M, Spiegelhalter D. Mapping the densities of malaria vectors within a single village. Acta Trop. 1995;59:1–18.CrossRefPubMed Smith T, Charlwood J, Takken W, Tanner M, Spiegelhalter D. Mapping the densities of malaria vectors within a single village. Acta Trop. 1995;59:1–18.CrossRefPubMed
19.
go back to reference Gillies M. Anopheline mosquitoes: vector behaviour and bionomics. Malaria: principles and practice of malariology. 1988;1:453–85. Gillies M. Anopheline mosquitoes: vector behaviour and bionomics. Malaria: principles and practice of malariology. 1988;1:453–85.
20.
go back to reference Midega JT, Smith DL, Olotu A, Mwangangi JM, Nzovu JG, Wambua J, et al. Wind direction and proximity to larval sites determines malaria risk in Kilifi District in Kenya. Nat Comm. 2012;3:674.CrossRef Midega JT, Smith DL, Olotu A, Mwangangi JM, Nzovu JG, Wambua J, et al. Wind direction and proximity to larval sites determines malaria risk in Kilifi District in Kenya. Nat Comm. 2012;3:674.CrossRef
21.
22.
go back to reference Ijumba JN, Mosha FW, Lindsay SW. Malaria transmission risk variations derived from different agricultural practices in an irrigated area of northern Tanzania. Med Vet Entomol. 2002;16:28–38.CrossRefPubMed Ijumba JN, Mosha FW, Lindsay SW. Malaria transmission risk variations derived from different agricultural practices in an irrigated area of northern Tanzania. Med Vet Entomol. 2002;16:28–38.CrossRefPubMed
23.
go back to reference Lindsay SW, Jawara M, Paine K, Pinder M, Walraven GEL, Emerson PM. Changes in house design reduce exposure to malaria mosquitoes. Trop Med Int Health. 2003;8:512–7.CrossRefPubMed Lindsay SW, Jawara M, Paine K, Pinder M, Walraven GEL, Emerson PM. Changes in house design reduce exposure to malaria mosquitoes. Trop Med Int Health. 2003;8:512–7.CrossRefPubMed
24.
go back to reference Santolamazza F, Calzetta M, Etang J, Barrese E, Dia I, Caccone A, et al. Distribution of knock-down resistance mutations in Anopheles gambiae molecular forms in west and west-central Africa. Malar J. 2008;7:e74.CrossRef Santolamazza F, Calzetta M, Etang J, Barrese E, Dia I, Caccone A, et al. Distribution of knock-down resistance mutations in Anopheles gambiae molecular forms in west and west-central Africa. Malar J. 2008;7:e74.CrossRef
25.
go back to reference Edi CV, Koudou BG, Jones CM, Weetman D, Ranson H. Multiple-insecticide resistance in Anopheles gambiae mosquitoes, Southern Cote d’Ivoire. Emerg Infect Dis. 2012;18:1508.CrossRefPubMedPubMedCentral Edi CV, Koudou BG, Jones CM, Weetman D, Ranson H. Multiple-insecticide resistance in Anopheles gambiae mosquitoes, Southern Cote d’Ivoire. Emerg Infect Dis. 2012;18:1508.CrossRefPubMedPubMedCentral
26.
go back to reference Antonio-Nkondjio C, Fossog BT, Ndo C, Djantio BM, Togouet SZ, Awono-Ambene P, et al. Anopheles gambiae distribution and insecticide resistance in the cities of Douala and Yaounde(Cameroon): influence of urban agriculture and pollution. Malar J. 2011;10:154.CrossRefPubMedPubMedCentral Antonio-Nkondjio C, Fossog BT, Ndo C, Djantio BM, Togouet SZ, Awono-Ambene P, et al. Anopheles gambiae distribution and insecticide resistance in the cities of Douala and Yaounde(Cameroon): influence of urban agriculture and pollution. Malar J. 2011;10:154.CrossRefPubMedPubMedCentral
27.
go back to reference Dabire K, Baldet T, Diabate A, Dia I, Costantini C, Cohuet A, et al. Anopheles funestus (Diptera: culicidae) in a humid savannah area of western Burkina Faso: bionomics, insecticide resistance status, and role in malaria transmission. J Med Entomol. 2007;44:990–7.CrossRefPubMed Dabire K, Baldet T, Diabate A, Dia I, Costantini C, Cohuet A, et al. Anopheles funestus (Diptera: culicidae) in a humid savannah area of western Burkina Faso: bionomics, insecticide resistance status, and role in malaria transmission. J Med Entomol. 2007;44:990–7.CrossRefPubMed
28.
go back to reference Casimiro S, Coleman M, Hemingway J, Sharp B. Insecticide resistance in Anopheles arabiensis and Anopheles gambiae from Mozambique. J Med Entomol. 2006;43:276–82.CrossRefPubMed Casimiro S, Coleman M, Hemingway J, Sharp B. Insecticide resistance in Anopheles arabiensis and Anopheles gambiae from Mozambique. J Med Entomol. 2006;43:276–82.CrossRefPubMed
29.
go back to reference Corbel V, N’Guessan R, Brengues C, Chandre F, Djogbenou L, Martin T, et al. Multiple insecticide resistance mechanisms in Anopheles gambiae and Culex quinquefasciatus from Benin, West Africa. Acta Trop. 2007;101:207–16.CrossRefPubMed Corbel V, N’Guessan R, Brengues C, Chandre F, Djogbenou L, Martin T, et al. Multiple insecticide resistance mechanisms in Anopheles gambiae and Culex quinquefasciatus from Benin, West Africa. Acta Trop. 2007;101:207–16.CrossRefPubMed
30.
go back to reference Coetzee M, van Wyk P, Booman M, Koekemoer LL, Hunt RH. Insecticide resistance in malaria vector mosquitoes in a gold mining town in Ghana and implications for malaria control. Bull Soc Path Exot. 2006;99:400–3. Coetzee M, van Wyk P, Booman M, Koekemoer LL, Hunt RH. Insecticide resistance in malaria vector mosquitoes in a gold mining town in Ghana and implications for malaria control. Bull Soc Path Exot. 2006;99:400–3.
31.
go back to reference Ochomo E, Bayoh NM, Kamau L, Atieli F, Vulule J, Ouma C, et al. Pyrethroid susceptibility of malaria vectors in four Districts of western Kenya. Parasit Vectors. 2014;7:310–8.CrossRefPubMedPubMedCentral Ochomo E, Bayoh NM, Kamau L, Atieli F, Vulule J, Ouma C, et al. Pyrethroid susceptibility of malaria vectors in four Districts of western Kenya. Parasit Vectors. 2014;7:310–8.CrossRefPubMedPubMedCentral
32.
go back to reference Zhou G, Afrane YA, Vardo-Zalik AM, Atieli H, Zhong D, Wamae P, et al. Changing patterns of malaria epidemiology between 2002 and 2010 in Western Kenya: the fall and rise of malaria. PLoS ONE. 2011;6:e20318.CrossRefPubMedPubMedCentral Zhou G, Afrane YA, Vardo-Zalik AM, Atieli H, Zhong D, Wamae P, et al. Changing patterns of malaria epidemiology between 2002 and 2010 in Western Kenya: the fall and rise of malaria. PLoS ONE. 2011;6:e20318.CrossRefPubMedPubMedCentral
33.
go back to reference N’Guessan R, Corbel V, Akogbeto M, Rowland M. Reduced efficacy of insecticide-treated nets and indoor residual spraying for malaria control in pyrethroid resistance area, Benin. Emerg Infect Dis. 2007;13:199–206.CrossRefPubMedPubMedCentral N’Guessan R, Corbel V, Akogbeto M, Rowland M. Reduced efficacy of insecticide-treated nets and indoor residual spraying for malaria control in pyrethroid resistance area, Benin. Emerg Infect Dis. 2007;13:199–206.CrossRefPubMedPubMedCentral
34.
go back to reference Molineaux L, Shidrawi G, Clarke J, Boulzaguet J, Ashkar T. Assessment of insecticidal impact on the malaria mosquito’s vectorial capacity, from data on the man-biting rate and age-composition. Bull World Health Organ. 1979;57:265.PubMedPubMedCentral Molineaux L, Shidrawi G, Clarke J, Boulzaguet J, Ashkar T. Assessment of insecticidal impact on the malaria mosquito’s vectorial capacity, from data on the man-biting rate and age-composition. Bull World Health Organ. 1979;57:265.PubMedPubMedCentral
35.
go back to reference Hargreaves K, Koekemoer L, Brooke B, Hunt R, Mthembu J, Coetzee M. Anopheles funestus resistant to pyrethroid insecticides in South Africa. Med Vet Entomol. 2000;14:181–9.CrossRefPubMed Hargreaves K, Koekemoer L, Brooke B, Hunt R, Mthembu J, Coetzee M. Anopheles funestus resistant to pyrethroid insecticides in South Africa. Med Vet Entomol. 2000;14:181–9.CrossRefPubMed
36.
go back to reference Garrett-Jones C, Grab B. The assessment of insecticidal impact on the malaria mosquito’s vectorial capacity, from data on the proportion of parous females. Bull World Health Organ. 1964;31:71.PubMedPubMedCentral Garrett-Jones C, Grab B. The assessment of insecticidal impact on the malaria mosquito’s vectorial capacity, from data on the proportion of parous females. Bull World Health Organ. 1964;31:71.PubMedPubMedCentral
37.
go back to reference Busvine J, Pal R. The impact of insecticide-resistance on control of vectors and vector-borne diseases. Bull World Health Organ. 1969;40:731.PubMedPubMedCentral Busvine J, Pal R. The impact of insecticide-resistance on control of vectors and vector-borne diseases. Bull World Health Organ. 1969;40:731.PubMedPubMedCentral
39.
go back to reference SAMCP. Kwazulu/Natal Malaria Crisis Progress Report. South Africa: KwaZulu/Natal Department of Health Statistics. 2001. SAMCP. Kwazulu/Natal Malaria Crisis Progress Report. South Africa: KwaZulu/Natal Department of Health Statistics. 2001.
40.
go back to reference Ceesay SJ, Casals-Pascual C, Nwakanma DC, Walther M, Gomez-Escobar N, Fulford AJ, et al. Continued decline of malaria in The Gambia with implications for elimination. PLoS ONE. 2010;5:e12242.CrossRefPubMedPubMedCentral Ceesay SJ, Casals-Pascual C, Nwakanma DC, Walther M, Gomez-Escobar N, Fulford AJ, et al. Continued decline of malaria in The Gambia with implications for elimination. PLoS ONE. 2010;5:e12242.CrossRefPubMedPubMedCentral
41.
go back to reference MoH. National Health Policy 2012–2020. In: Welfare MoHaS, editor. Banjul: Ministry of Health and Social Welfare; 2012. p. 22. MoH. National Health Policy 2012–2020. In: Welfare MoHaS, editor. Banjul: Ministry of Health and Social Welfare; 2012. p. 22.
42.
go back to reference Tangena J, Adiamoh M, D’Alessandro U, Jarju L, Jawara M, Jeffries D, et al. Alternative treatments for indoor residual spraying for malaria control in a village with pyrethroid-and DDT-resistant vectors in the Gambia. PLoS ONE. 2013;8:e74351.CrossRefPubMedPubMedCentral Tangena J, Adiamoh M, D’Alessandro U, Jarju L, Jawara M, Jeffries D, et al. Alternative treatments for indoor residual spraying for malaria control in a village with pyrethroid-and DDT-resistant vectors in the Gambia. PLoS ONE. 2013;8:e74351.CrossRefPubMedPubMedCentral
43.
go back to reference Pinder M, Jawara M, Jarju LB, Salami K, Jeffries D, Adiamoh M, et al. Efficacy of indoor residual spraying with dichlorodiphenyltrichloroethane against malaria in Gambian communities with high usage of long-lasting insecticidal mosquito nets: a cluster-randomised controlled trial. Lancet. 2014;385:1436–46.CrossRefPubMed Pinder M, Jawara M, Jarju LB, Salami K, Jeffries D, Adiamoh M, et al. Efficacy of indoor residual spraying with dichlorodiphenyltrichloroethane against malaria in Gambian communities with high usage of long-lasting insecticidal mosquito nets: a cluster-randomised controlled trial. Lancet. 2014;385:1436–46.CrossRefPubMed
44.
go back to reference Caputo B, Nwakanma D, Jawara M, Adiamoh M, Dia I, Konate L, et al. Anopheles gambiae complex along The Gambia river, with particular reference to the molecular forms of An. gambiae s.s. Malar J. 2008;7:182.CrossRefPubMedPubMedCentral Caputo B, Nwakanma D, Jawara M, Adiamoh M, Dia I, Konate L, et al. Anopheles gambiae complex along The Gambia river, with particular reference to the molecular forms of An. gambiae s.s. Malar J. 2008;7:182.CrossRefPubMedPubMedCentral
45.
go back to reference Majambere S, Fillinger U, Sayer DR, Green C, Lindsay SW. Spatial distribution of mosquito larvae and the potential for targeted larval control in The Gambia. Am J Trop Med Hyg. 2008;79:19–27.PubMed Majambere S, Fillinger U, Sayer DR, Green C, Lindsay SW. Spatial distribution of mosquito larvae and the potential for targeted larval control in The Gambia. Am J Trop Med Hyg. 2008;79:19–27.PubMed
46.
go back to reference Bryan J, Petrarca V, Di Deco M, Coluzzi M. Adult behaviour of members of the Anopheles gambiae complex in the Gambia with special reference to An. melas and its chromosomal variants. Parassitologia. 1986;29:221–49. Bryan J, Petrarca V, Di Deco M, Coluzzi M. Adult behaviour of members of the Anopheles gambiae complex in the Gambia with special reference to An. melas and its chromosomal variants. Parassitologia. 1986;29:221–49.
47.
go back to reference Reimer L, Tripet F, Slotman M, Spielman A, Fondjo E, Lanzaro G. An unusual distribution of the kdr gene among populations of Anopheles gambiae on the island of Bioko, Equatorial Guinea. Insect Mol Biol. 2005;14:683–8.CrossRefPubMed Reimer L, Tripet F, Slotman M, Spielman A, Fondjo E, Lanzaro G. An unusual distribution of the kdr gene among populations of Anopheles gambiae on the island of Bioko, Equatorial Guinea. Insect Mol Biol. 2005;14:683–8.CrossRefPubMed
48.
go back to reference Dabiré KR, Diabaté A, Djogbenou L, Ouari A, N’Guessan R, Ouédraogo J-B, et al. Dynamics of multiple insecticide resistance in the malaria vector Anopheles gambiae in a rice growing area in South-Western Burkina Faso. Malar J. 2008;7:188.CrossRefPubMedPubMedCentral Dabiré KR, Diabaté A, Djogbenou L, Ouari A, N’Guessan R, Ouédraogo J-B, et al. Dynamics of multiple insecticide resistance in the malaria vector Anopheles gambiae in a rice growing area in South-Western Burkina Faso. Malar J. 2008;7:188.CrossRefPubMedPubMedCentral
49.
go back to reference Djègbè I, Boussari O, Sidick A, Martin T, Ranson H, Chandre F, et al. Dynamics of insecticide resistance in malaria vectors in Benin: first evidence of the presence of L1014S kdr mutation in Anopheles gambiae from West Africa. Malar J. 2011;10:261.CrossRefPubMedPubMedCentral Djègbè I, Boussari O, Sidick A, Martin T, Ranson H, Chandre F, et al. Dynamics of insecticide resistance in malaria vectors in Benin: first evidence of the presence of L1014S kdr mutation in Anopheles gambiae from West Africa. Malar J. 2011;10:261.CrossRefPubMedPubMedCentral
50.
go back to reference Costantini C, Ayala D, Guelbeogo WM, Pombi M, Some CY, Bassole IH, et al. Living at the edge: biogeographic patterns of habitat segregation conform to speciation by niche expansion in Anopheles gambiae. BMC Ecol. 2009;9:16.CrossRefPubMedPubMedCentral Costantini C, Ayala D, Guelbeogo WM, Pombi M, Some CY, Bassole IH, et al. Living at the edge: biogeographic patterns of habitat segregation conform to speciation by niche expansion in Anopheles gambiae. BMC Ecol. 2009;9:16.CrossRefPubMedPubMedCentral
51.
go back to reference Gimonneau G, Pombi M, Choisy M, Morand S, Dabiré RK, Simard F. Larval habitat segregation between the molecular forms of the mosquito Anopheles gambiae in a rice field area of Burkina Faso, West Africa. Med Vet Entomol. 2012;26:9–17.CrossRefPubMedPubMedCentral Gimonneau G, Pombi M, Choisy M, Morand S, Dabiré RK, Simard F. Larval habitat segregation between the molecular forms of the mosquito Anopheles gambiae in a rice field area of Burkina Faso, West Africa. Med Vet Entomol. 2012;26:9–17.CrossRefPubMedPubMedCentral
52.
go back to reference Taylor C, Touré YT, Carnahan J, Norris DE, Dolo G, Traoré SF, et al. Gene flow among populations of the malaria vector, Anopheles gambiae, in Mali, West Africa. Genetics. 2001;157:743–50.PubMedPubMedCentral Taylor C, Touré YT, Carnahan J, Norris DE, Dolo G, Traoré SF, et al. Gene flow among populations of the malaria vector, Anopheles gambiae, in Mali, West Africa. Genetics. 2001;157:743–50.PubMedPubMedCentral
53.
go back to reference Clarkson CS, Weetman D, Essandoh J, Yawson AE, Maslen G, Manske M, et al. Adaptive introgression between Anopheles sibling species eliminates a major genomic island but not reproductive isolation. Nat Comm. 2014;5:4248.CrossRef Clarkson CS, Weetman D, Essandoh J, Yawson AE, Maslen G, Manske M, et al. Adaptive introgression between Anopheles sibling species eliminates a major genomic island but not reproductive isolation. Nat Comm. 2014;5:4248.CrossRef
54.
go back to reference Weetman D, Wilding CS, Steen K, Pinto J, Donnelly MJ. Gene flow–dependent genomic divergence between Anopheles gambiae M and S forms. Mol Biol Evol. 2012;29:279–91.CrossRefPubMedPubMedCentral Weetman D, Wilding CS, Steen K, Pinto J, Donnelly MJ. Gene flow–dependent genomic divergence between Anopheles gambiae M and S forms. Mol Biol Evol. 2012;29:279–91.CrossRefPubMedPubMedCentral
55.
go back to reference Chandre F, Manguin S, Brengues C, Dossou YJ, Darriet F, Diabate A, et al. Current distribution of a pyrethroid resistance gene (kdr) in Anopheles gambiae complex from west Africa and further evidence for reproductive isolation of the Mopti form. Parassitologia. 1999;41:319–22.PubMed Chandre F, Manguin S, Brengues C, Dossou YJ, Darriet F, Diabate A, et al. Current distribution of a pyrethroid resistance gene (kdr) in Anopheles gambiae complex from west Africa and further evidence for reproductive isolation of the Mopti form. Parassitologia. 1999;41:319–22.PubMed
56.
go back to reference Weill M, Chandre F, Brengues C, Manguin S, Akogbeto M, Pasteur N, et al. The kdr mutation occurs in the Mopti form of Anopheles gambiae s.s. through introgression. Insect Mol Biol. 2000;9:451–5.CrossRefPubMed Weill M, Chandre F, Brengues C, Manguin S, Akogbeto M, Pasteur N, et al. The kdr mutation occurs in the Mopti form of Anopheles gambiae s.s. through introgression. Insect Mol Biol. 2000;9:451–5.CrossRefPubMed
58.
go back to reference WHO. Test procedures for insecticide resistance monitoring in malaria vector mosquitoes. Geneva: World Health Organization. 2013. WHO. Test procedures for insecticide resistance monitoring in malaria vector mosquitoes. Geneva: World Health Organization. 2013.
59.
go back to reference Scott JA, Brogdon WG, Collins FH. Identification of single specimens of the Anopheles gambiae complex by the Polymerase Chain Reaction. Am J Trop Med Hyg. 1993;49:520–9.PubMed Scott JA, Brogdon WG, Collins FH. Identification of single specimens of the Anopheles gambiae complex by the Polymerase Chain Reaction. Am J Trop Med Hyg. 1993;49:520–9.PubMed
60.
go back to reference Santolamazza F, Mancini E, Simard F, Qi Y, Tu Z, Della Torre A. Insertion polymorphisms of SINE200 retrotransposons within speciation islands of Anopheles gambiae molecular forms. Malar J. 2008;7:163.CrossRefPubMedPubMedCentral Santolamazza F, Mancini E, Simard F, Qi Y, Tu Z, Della Torre A. Insertion polymorphisms of SINE200 retrotransposons within speciation islands of Anopheles gambiae molecular forms. Malar J. 2008;7:163.CrossRefPubMedPubMedCentral
61.
go back to reference Bass C, Williamson MS, Wilding CS, Donnelly MJ, Field LM. Identification of the main malaria vectors in the Anopheles gambiae species complex using a TaqMan real-time PCR assay. Malar J. 2007;6:155.CrossRefPubMedPubMedCentral Bass C, Williamson MS, Wilding CS, Donnelly MJ, Field LM. Identification of the main malaria vectors in the Anopheles gambiae species complex using a TaqMan real-time PCR assay. Malar J. 2007;6:155.CrossRefPubMedPubMedCentral
62.
go back to reference Bass C, Nikou D, Vontas J, Williamson MS, Field LM. Development of high-throughput real-time PCR assays for the identification of insensitive acetylcholinesterase (ace-1R) in Anopheles gambiae. Pest Biochem Physiol. 2010;96:80–5.CrossRef Bass C, Nikou D, Vontas J, Williamson MS, Field LM. Development of high-throughput real-time PCR assays for the identification of insensitive acetylcholinesterase (ace-1R) in Anopheles gambiae. Pest Biochem Physiol. 2010;96:80–5.CrossRef
63.
go back to reference Jones CM, Liyanapathirana M, Agossa FR, Weetman D, Ranson H, Donnelly MJ, et al. Footprints of positive selection associated with a mutation (N1575Y) in the voltage-gated sodium channel of Anopheles gambiae. Proc Natl Acad Sci USA. 2012;109:6614–9.CrossRefPubMedPubMedCentral Jones CM, Liyanapathirana M, Agossa FR, Weetman D, Ranson H, Donnelly MJ, et al. Footprints of positive selection associated with a mutation (N1575Y) in the voltage-gated sodium channel of Anopheles gambiae. Proc Natl Acad Sci USA. 2012;109:6614–9.CrossRefPubMedPubMedCentral
64.
go back to reference Mitchell SN, Rigden DJ, Dowd AJ, Lu F, Wilding CS, Weetman D, et al. Metabolic and Target-Site Mechanisms Combine to Confer Strong DDT Resistance in Anopheles gambiae. PLoS ONE. 2014;9:e92662.CrossRefPubMedPubMedCentral Mitchell SN, Rigden DJ, Dowd AJ, Lu F, Wilding CS, Weetman D, et al. Metabolic and Target-Site Mechanisms Combine to Confer Strong DDT Resistance in Anopheles gambiae. PLoS ONE. 2014;9:e92662.CrossRefPubMedPubMedCentral
66.
go back to reference Newcombe RG. Two-sided confidence intervals for the single proportion: comparison of seven methods. Stat Med. 1998;17:857–72.CrossRefPubMed Newcombe RG. Two-sided confidence intervals for the single proportion: comparison of seven methods. Stat Med. 1998;17:857–72.CrossRefPubMed
67.
go back to reference Wilson EB. Probable inference, the law of succession, and statistical inference. J Am Stat Assoc. 1927;22:209–12.CrossRef Wilson EB. Probable inference, the law of succession, and statistical inference. J Am Stat Assoc. 1927;22:209–12.CrossRef
68.
go back to reference Thomson M, d’Alessandro U, Bennett S, Connor S, Langerock P, Jawara M, et al. Malaria prevalence is inversely related to vector density in The Gambia, West Africa. Trans R Soc Trop Med Hyg. 1994;88:638–43.CrossRefPubMed Thomson M, d’Alessandro U, Bennett S, Connor S, Langerock P, Jawara M, et al. Malaria prevalence is inversely related to vector density in The Gambia, West Africa. Trans R Soc Trop Med Hyg. 1994;88:638–43.CrossRefPubMed
69.
go back to reference Okebe J, Affara M, Correa S, Muhammad AK, Nwakanma D, Drakeley C, et al. School-Based Countrywide Seroprevalence Survey Reveals Spatial Heterogeneity in Malaria Transmission in the Gambia. PLoS ONE. 2014;9:e110926.CrossRefPubMedPubMedCentral Okebe J, Affara M, Correa S, Muhammad AK, Nwakanma D, Drakeley C, et al. School-Based Countrywide Seroprevalence Survey Reveals Spatial Heterogeneity in Malaria Transmission in the Gambia. PLoS ONE. 2014;9:e110926.CrossRefPubMedPubMedCentral
70.
go back to reference Henry M-C, Assi S-B, Rogier C, Dossou-Yovo J, Chandre F, Guillet P, et al. Protective efficacy of lambda-cyhalothrin treated nets in Anopheles gambiae pyrethroid resistance areas of Cote d’Ivoire. Am J Trop Med Hyg. 2005;73:859–64.PubMed Henry M-C, Assi S-B, Rogier C, Dossou-Yovo J, Chandre F, Guillet P, et al. Protective efficacy of lambda-cyhalothrin treated nets in Anopheles gambiae pyrethroid resistance areas of Cote d’Ivoire. Am J Trop Med Hyg. 2005;73:859–64.PubMed
71.
go back to reference Wondji CS, Coleman M, Kleinschmidt I, Mzilahowa T, Irving H, Ndula M, et al. Impact of pyrethroid resistance on operational malaria control in Malawi. Proc Natl Acad Sci USA. 2012;109:19063–70.CrossRefPubMedPubMedCentral Wondji CS, Coleman M, Kleinschmidt I, Mzilahowa T, Irving H, Ndula M, et al. Impact of pyrethroid resistance on operational malaria control in Malawi. Proc Natl Acad Sci USA. 2012;109:19063–70.CrossRefPubMedPubMedCentral
72.
go back to reference Tokponnon FT, Ogouyémi AH, Sissinto Y, Sovi A, Gnanguenon V, Cornélie S, et al. Impact of long-lasting, insecticidal nets on anaemia and prevalence of Plasmodium falciparum among children under five years in areas with highly resistant malaria vectors. Malar J. 2014;13:76.CrossRefPubMedPubMedCentral Tokponnon FT, Ogouyémi AH, Sissinto Y, Sovi A, Gnanguenon V, Cornélie S, et al. Impact of long-lasting, insecticidal nets on anaemia and prevalence of Plasmodium falciparum among children under five years in areas with highly resistant malaria vectors. Malar J. 2014;13:76.CrossRefPubMedPubMedCentral
73.
go back to reference Lindblade KA, Mwandama D, Mzilahowa T, Steinhardt L, Gimnig J, Shah M, et al. A cohort study of the effectiveness of insecticide-treated bed nets to prevent malaria in an area of moderate pyrethroid resistance, Malawi. Malar J. 2015;14:31.CrossRefPubMedPubMedCentral Lindblade KA, Mwandama D, Mzilahowa T, Steinhardt L, Gimnig J, Shah M, et al. A cohort study of the effectiveness of insecticide-treated bed nets to prevent malaria in an area of moderate pyrethroid resistance, Malawi. Malar J. 2015;14:31.CrossRefPubMedPubMedCentral
74.
go back to reference Trape J-F, Tall A, Diagne N, Ndiath O, Ly AB, Faye J, et al. Malaria morbidity and pyrethroid resistance after the introduction of insecticide-treated bednets and artemisinin-based combination therapies: a longitudinal study. Lancet Infect Dis. 2011;11:925–32.CrossRefPubMed Trape J-F, Tall A, Diagne N, Ndiath O, Ly AB, Faye J, et al. Malaria morbidity and pyrethroid resistance after the introduction of insecticide-treated bednets and artemisinin-based combination therapies: a longitudinal study. Lancet Infect Dis. 2011;11:925–32.CrossRefPubMed
75.
go back to reference Kleinschmidt I, Mnzava AP, Kafy HT, Mbogo C, Bashir AI, Bigoga J, et al. Design of a study to determine the impact of insecticide resistance on malaria vector control: a multi-country investigation. Malar J. 2015;14:282.CrossRefPubMedPubMedCentral Kleinschmidt I, Mnzava AP, Kafy HT, Mbogo C, Bashir AI, Bigoga J, et al. Design of a study to determine the impact of insecticide resistance on malaria vector control: a multi-country investigation. Malar J. 2015;14:282.CrossRefPubMedPubMedCentral
76.
go back to reference Jawara M, Pinder M, Drakeley CJ, Nwakanma DC, Jallow E, Bogh C, et al. Dry season ecology of Anopheles gambiae complex mosquitoes in The Gambia. Malar J. 2008;7:9.CrossRef Jawara M, Pinder M, Drakeley CJ, Nwakanma DC, Jallow E, Bogh C, et al. Dry season ecology of Anopheles gambiae complex mosquitoes in The Gambia. Malar J. 2008;7:9.CrossRef
77.
go back to reference Lindsay S, Alonso P, Schellenberg JA, Hemingway J, Adiamah J, Shenton F, et al. A malaria control trial using insecticide-treated bed nets and targeted chemoprophylaxis in a rural area of The Gambia, west Africa 7. Impact of permethrin-impregnated bed nets on malaria vectors. Trans R Soc Trop Med Hyg. 1993;87(Suppl 2):45–51.CrossRefPubMed Lindsay S, Alonso P, Schellenberg JA, Hemingway J, Adiamah J, Shenton F, et al. A malaria control trial using insecticide-treated bed nets and targeted chemoprophylaxis in a rural area of The Gambia, west Africa 7. Impact of permethrin-impregnated bed nets on malaria vectors. Trans R Soc Trop Med Hyg. 1993;87(Suppl 2):45–51.CrossRefPubMed
78.
go back to reference Bryan J, Di Deco M, Petrarca V, Coluzzi M. Inversion polymorphism and incipient speciation in Anopheles gambiae s.s. in the Gambia, West Africa. Genetica. 1982;59:167–76.CrossRef Bryan J, Di Deco M, Petrarca V, Coluzzi M. Inversion polymorphism and incipient speciation in Anopheles gambiae s.s. in the Gambia, West Africa. Genetica. 1982;59:167–76.CrossRef
79.
go back to reference Mawejje HD, Wilding CS, Rippon EJ, Hughes A, Weetman D, Donnelly MJ. Insecticide resistance monitoring of field-collected Anopheles gambiae s.l. populations from Jinja, eastern Uganda, identifies high levels of pyrethroid resistance. Med Vet Entomol. 2013;27:276–83.CrossRefPubMedPubMedCentral Mawejje HD, Wilding CS, Rippon EJ, Hughes A, Weetman D, Donnelly MJ. Insecticide resistance monitoring of field-collected Anopheles gambiae s.l. populations from Jinja, eastern Uganda, identifies high levels of pyrethroid resistance. Med Vet Entomol. 2013;27:276–83.CrossRefPubMedPubMedCentral
80.
go back to reference Reimer L, Fondjo E, Patchoke S, Diallo B, Lee Y, Ng A, et al. Relationship between kdr mutation and resistance to pyrethroid and DDT insecticides in natural populations of Anopheles gambiae. J Med Entomol. 2008;45:260–6.CrossRefPubMed Reimer L, Fondjo E, Patchoke S, Diallo B, Lee Y, Ng A, et al. Relationship between kdr mutation and resistance to pyrethroid and DDT insecticides in natural populations of Anopheles gambiae. J Med Entomol. 2008;45:260–6.CrossRefPubMed
81.
go back to reference Pinder M, Jawara M, Jarju LB, Kandeh B, Jeffries D, Lluberas MF, et al. To assess whether indoor residual spraying can provide additional protection against clinical malaria over current best practice of long-lasting insecticidal mosquito nets in The Gambia: study protocol for a two-armed cluster-randomised trial. Trials. 2011;12:147.CrossRefPubMedPubMedCentral Pinder M, Jawara M, Jarju LB, Kandeh B, Jeffries D, Lluberas MF, et al. To assess whether indoor residual spraying can provide additional protection against clinical malaria over current best practice of long-lasting insecticidal mosquito nets in The Gambia: study protocol for a two-armed cluster-randomised trial. Trials. 2011;12:147.CrossRefPubMedPubMedCentral
82.
go back to reference SNMCP. Profil entomologique du paludisme au Senegal: Ministere de la Sante et de la prevention Medicale Profil. 2011. SNMCP. Profil entomologique du paludisme au Senegal: Ministere de la Sante et de la prevention Medicale Profil. 2011.
83.
go back to reference Niang E. A. Variabilité génétique des populations d’Anopheles gambiae s.l. au Sénégal: implications dans le contrôle du paludisme. Cheikh Anta Diop de Dakar. 2014. Niang E. A. Variabilité génétique des populations d’Anopheles gambiae s.l. au Sénégal: implications dans le contrôle du paludisme. Cheikh Anta Diop de Dakar. 2014.
84.
go back to reference Padonou G, Sezonlin M, Gbedjissi G, Ayi I, Azondekon R, Djenontin A, et al. Biology of Anopheles gambiae and insecticide resistance: entomological study for a large scale of indoor residual spraying in south east Benin. J Parasitol Vector Biol. 2011;3:59–68. Padonou G, Sezonlin M, Gbedjissi G, Ayi I, Azondekon R, Djenontin A, et al. Biology of Anopheles gambiae and insecticide resistance: entomological study for a large scale of indoor residual spraying in south east Benin. J Parasitol Vector Biol. 2011;3:59–68.
85.
go back to reference Kloke RG, Nhamahanga E, Hunt RH, Coetzee M. Vectorial status and insecticide resistance of Anopheles funestus from a sugar estate in southern Mozambique. Parasit Vectors. 2011;4:16.CrossRefPubMedPubMedCentral Kloke RG, Nhamahanga E, Hunt RH, Coetzee M. Vectorial status and insecticide resistance of Anopheles funestus from a sugar estate in southern Mozambique. Parasit Vectors. 2011;4:16.CrossRefPubMedPubMedCentral
86.
go back to reference Stump AD, Atieli FK, Vulule JM, Besansky NJ. Dynamics of the pyrethroid knockdown resistance allele in western Kenyan populations of Anopheles gambiae in response to insecticide-treated bed net trials. Am J Trop Med Hyg. 2004;70:591–6.PubMed Stump AD, Atieli FK, Vulule JM, Besansky NJ. Dynamics of the pyrethroid knockdown resistance allele in western Kenyan populations of Anopheles gambiae in response to insecticide-treated bed net trials. Am J Trop Med Hyg. 2004;70:591–6.PubMed
87.
go back to reference de Zulueta J. Insecticide resistance in Anopheles sacharovi. Bull World Health Organ. 1959;20:797.PubMedCentral de Zulueta J. Insecticide resistance in Anopheles sacharovi. Bull World Health Organ. 1959;20:797.PubMedCentral
88.
go back to reference Diatta M, Spiegel A, Lochouarn L, Fontenille D. Similar feeding preferences of Anopheles gambiae and A. arabiensis in Senegal. Trans R Soc Trop Med Hyg. 1998;92:270–2.CrossRefPubMed Diatta M, Spiegel A, Lochouarn L, Fontenille D. Similar feeding preferences of Anopheles gambiae and A. arabiensis in Senegal. Trans R Soc Trop Med Hyg. 1998;92:270–2.CrossRefPubMed
89.
go back to reference Ndiath MO, Mazenot C, Sokhna C, Trape JF. How the malaria vector Anopheles gambiae adapts to the use of insecticide-treated nets by African populations. PLoS ONE. 2014;9:e97700.CrossRefPubMedPubMedCentral Ndiath MO, Mazenot C, Sokhna C, Trape JF. How the malaria vector Anopheles gambiae adapts to the use of insecticide-treated nets by African populations. PLoS ONE. 2014;9:e97700.CrossRefPubMedPubMedCentral
Metadata
Title
Does insecticide resistance contribute to heterogeneities in malaria transmission in The Gambia?
Authors
Kevin Ochieng’ Opondo
David Weetman
Musa Jawara
Mathurin Diatta
Amfaal Fofana
Florence Crombe
Julia Mwesigwa
Umberto D’Alessandro
Martin James Donnelly
Publication date
01-12-2016
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2016
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-016-1203-z

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