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Published in: Malaria Journal 1/2020

01-12-2020 | Malaria | Research

Insecticide resistance in indoor and outdoor-resting Anopheles gambiae in Northern Ghana

Authors: Majidah Hamid-Adiamoh, Alfred Amambua-Ngwa, Davis Nwakanma, Umberto D’Alessandro, Gordon A. Awandare, Yaw A. Afrane

Published in: Malaria Journal | Issue 1/2020

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Abstract

Background

Selection pressure from continued exposure to insecticides drives development of insecticide resistance and changes in resting behaviour of malaria vectors. There is need to understand how resistance drives changes in resting behaviour within vector species. The association between insecticide resistance and resting behaviour of Anopheles gambiae sensu lato (s.l.) in Northern Ghana was examined.

Methods

F1 progenies from adult mosquitoes collected indoors and outdoors were exposed to DDT, deltamethrin, malathion and bendiocarb using WHO insecticide susceptibility tests. Insecticide resistance markers including voltage-gated sodium channel (Vgsc)-1014F, Vgsc-1014S, Vgsc-1575Y, glutathione-S-transferase epsilon 2 (GSTe2)-114T and acetylcholinesterase (Ace1)-119S, as well as blood meal sources were investigated using PCR methods. Activities of metabolic enzymes, acetylcholine esterase (AChE), non-specific β-esterases, glutathione-S-transferase (GST) and monooxygenases were measured from unexposed F1 progenies using microplate assays.

Results

Susceptibility of Anopheles coluzzii to deltamethrin 24 h post-exposure was significantly higher in indoor (mortality = 5%) than outdoor (mortality = 2.5%) populations (P = 0.02). Mosquitoes were fully susceptible to malathion (mortality: indoor = 98%, outdoor = 100%). Susceptibility to DDT was significantly higher in outdoor (mortality = 9%) than indoor (mortality = 0%) mosquitoes (P = 0.006). Mosquitoes were also found with suspected resistance to bendiocarb but mortality was not statistically different (mortality: indoor = 90%, outdoor = 95%. P = 0.30). Frequencies of all resistance alleles were higher in F1 outdoor (0.11–0.85) than indoor (0.04–0.65) mosquito populations, while Vgsc-1014F in F0 An. gambiae sensu stricto (s.s) was significantly associated with outdoor-resting behaviour (P = 0.01). Activities of non-specific β-esterase enzymes were significantly higher in outdoor than indoor mosquitoes (Mean enzyme activity: Outdoor = : 1.70/mg protein; Indoor = 1.35/mg protein. P < 0.0001). AChE activity was also more elevated in outdoor (0.62/mg protein) than indoor (0.57/mg protein) mosquitoes but this was not significant (P = 0.08). Human blood index (HBI) was predominantly detected in indoor (18%) than outdoor mosquito populations (3%).

Conclusions

The overall results did not establish that there was a significant preference of resistant malaria vectors to solely rest indoors or outdoors, but varied depending on the resistant alleles present. Phenotypic resistance was higher in indoor than outdoor-resting mosquitoes, but genotypic and metabolic resistance levels were higher in outdoor than the indoor populations. Continued monitoring of changes in resting behaviour within An. gambiae s.l. populations is recommended.
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Literature
1.
go back to reference WHO. Global malaria programme. Global technical strategy for malaria, 2016–2030. Geneva: World Health Organization; 2015. WHO. Global malaria programme. Global technical strategy for malaria, 2016–2030. Geneva: World Health Organization; 2015.
2.
go back to reference WHO. World malaria report 2019. Geneva: World Health Organization; 2019. WHO. World malaria report 2019. Geneva: World Health Organization; 2019.
3.
go back to reference Hemingway J, Ranson H. Insecticide resistance in insect vectors of human diseases. Annu Rev Entomol. 2000;45:371–91.PubMed Hemingway J, Ranson H. Insecticide resistance in insect vectors of human diseases. Annu Rev Entomol. 2000;45:371–91.PubMed
5.
go back to reference Sokhna C, Ndiath MO, Rogier C. The changes in mosquito vector behaviour and the emerging resistance to insecticides will challenge the decline of malaria. Clin Microbiol Infect. 2013;19:902–7.PubMed Sokhna C, Ndiath MO, Rogier C. The changes in mosquito vector behaviour and the emerging resistance to insecticides will challenge the decline of malaria. Clin Microbiol Infect. 2013;19:902–7.PubMed
6.
go back to reference Huho B, Briët O, Seyoum A, Sikaala C, Bayoh N, Gimnig J, et al. Consistently high estimates for the proportion of human exposure to malaria vector populations occurring indoors in rural Africa. Int J Epidemiol. 2013;42:235–47.PubMedPubMedCentral Huho B, Briët O, Seyoum A, Sikaala C, Bayoh N, Gimnig J, et al. Consistently high estimates for the proportion of human exposure to malaria vector populations occurring indoors in rural Africa. Int J Epidemiol. 2013;42:235–47.PubMedPubMedCentral
7.
go back to reference Pluess B, Tanser FC, Lengeler C, Sharp BL. Indoor residual spraying for preventing malaria. Cochrane Database Syst Rev. 2010;4:CD006657. Pluess B, Tanser FC, Lengeler C, Sharp BL. Indoor residual spraying for preventing malaria. Cochrane Database Syst Rev. 2010;4:CD006657.
8.
go back to reference Russell TL, Govella NJ, Azizi S, Drakeley CJ, Kachur SP, Killeen GF. Increased proportions of outdoor feeding among residual malaria vector populations following increased use of insecticide-treated nets in rural Tanzania. Malar J. 2011;10:80.PubMedPubMedCentral Russell TL, Govella NJ, Azizi S, Drakeley CJ, Kachur SP, Killeen GF. Increased proportions of outdoor feeding among residual malaria vector populations following increased use of insecticide-treated nets in rural Tanzania. Malar J. 2011;10:80.PubMedPubMedCentral
9.
go back to reference Thomsen EK, Koimbu G, Pulford J, Jamea-Maiasa S, Ura Y, Keven JB, et al. Mosquito behavior change after distribution of bednets results in decreased protection against malaria exposure. J Infect Dis. 2017;215:790–7.PubMed Thomsen EK, Koimbu G, Pulford J, Jamea-Maiasa S, Ura Y, Keven JB, et al. Mosquito behavior change after distribution of bednets results in decreased protection against malaria exposure. J Infect Dis. 2017;215:790–7.PubMed
10.
go back to reference Meyers JI, Pathikonda S, Popkin-Hall ZR, Medeiros MC, Fuseini G, Matias A, et al. Increasing outdoor host-seeking in Anopheles gambiae over 6 years of vector control on Bioko Island. Malar J. 2016;15:239.PubMedPubMedCentral Meyers JI, Pathikonda S, Popkin-Hall ZR, Medeiros MC, Fuseini G, Matias A, et al. Increasing outdoor host-seeking in Anopheles gambiae over 6 years of vector control on Bioko Island. Malar J. 2016;15:239.PubMedPubMedCentral
11.
go back to reference Tchouassi DP, Quakyi IA, Addison EA, Bosompem KM, Wilson MD, Appawu MA, et al. Characterization of malaria transmission by vector populations for improved interventions during the dry season in the Kpone-on-Sea area of coastal Ghana. Parasit Vectors. 2012;5:212.PubMedPubMedCentral Tchouassi DP, Quakyi IA, Addison EA, Bosompem KM, Wilson MD, Appawu MA, et al. Characterization of malaria transmission by vector populations for improved interventions during the dry season in the Kpone-on-Sea area of coastal Ghana. Parasit Vectors. 2012;5:212.PubMedPubMedCentral
12.
go back to reference Trape JF, 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.PubMed Trape JF, 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.PubMed
13.
go back to reference Degefa T, Yewhalaw D, Zhou G, Lee MC, Atieli H, Githeko AK, et al. Indoor and outdoor malaria vector surveillance in western Kenya: implications for better understanding of residual transmission. Malar J. 2017;16:443.PubMedPubMedCentral Degefa T, Yewhalaw D, Zhou G, Lee MC, Atieli H, Githeko AK, et al. Indoor and outdoor malaria vector surveillance in western Kenya: implications for better understanding of residual transmission. Malar J. 2017;16:443.PubMedPubMedCentral
14.
go back to reference Ototo EN, Mbugi JP, Wanjala CL, Zhou G, Githeko AK, Yan G. Surveillance of malaria vector population density and biting behaviour in western Kenya. Malar J. 2015;14:244.PubMedPubMedCentral Ototo EN, Mbugi JP, Wanjala CL, Zhou G, Githeko AK, Yan G. Surveillance of malaria vector population density and biting behaviour in western Kenya. Malar J. 2015;14:244.PubMedPubMedCentral
15.
go back to reference Akogbéto MC, Salako AS, Dagnon F, Aïkpon R, Kouletio M, Sovi A, et al. Blood feeding behaviour comparison and contribution of Anopheles coluzzii and Anopheles gambiae, two sibling species living in sympatry, to malaria transmission in Alibori and Donga region, northern Benin, West Africa. Malar J. 2018;17:307.PubMedPubMedCentral Akogbéto MC, Salako AS, Dagnon F, Aïkpon R, Kouletio M, Sovi A, et al. Blood feeding behaviour comparison and contribution of Anopheles coluzzii and Anopheles gambiae, two sibling species living in sympatry, to malaria transmission in Alibori and Donga region, northern Benin, West Africa. Malar J. 2018;17:307.PubMedPubMedCentral
16.
go back to reference Kibret S, Wilson GG. Increased outdoor biting tendency of Anopheles arabiensis and its challenge for malaria control in Central Ethiopia. Public Health. 2016;141:143–5.PubMed Kibret S, Wilson GG. Increased outdoor biting tendency of Anopheles arabiensis and its challenge for malaria control in Central Ethiopia. Public Health. 2016;141:143–5.PubMed
17.
go back to reference Mourou J-R, Coffinet T, Jarjaval F, Cotteaux C, Pradines E, Godefroy L, et al. Malaria transmission in Libreville: results of a one year survey. Malar J. 2012;11:40.PubMedPubMedCentral Mourou J-R, Coffinet T, Jarjaval F, Cotteaux C, Pradines E, Godefroy L, et al. Malaria transmission in Libreville: results of a one year survey. Malar J. 2012;11:40.PubMedPubMedCentral
18.
go back to reference Clarkson CS, Miles A, Harding NJ, Weetman D, Kwiatkowski D, Donnelly M, et al. The genetic architecture of target-site resistance to pyrethroid insecticides in the African malaria vectors Anopheles gambiae and Anopheles coluzzii. bioRxiv. 2018. Clarkson CS, Miles A, Harding NJ, Weetman D, Kwiatkowski D, Donnelly M, et al. The genetic architecture of target-site resistance to pyrethroid insecticides in the African malaria vectors Anopheles gambiae and Anopheles coluzzii. bioRxiv. 2018.
19.
go back to reference Djègbè I, Agossa FR, Jones CM, Poupardin R, Cornelie S, Akogbéto M, et al. Molecular characterization of DDT resistance in Anopheles gambiae from Benin. Parasit Vectors. 2014;7:409.PubMedPubMedCentral Djègbè I, Agossa FR, Jones CM, Poupardin R, Cornelie S, Akogbéto M, et al. Molecular characterization of DDT resistance in Anopheles gambiae from Benin. Parasit Vectors. 2014;7:409.PubMedPubMedCentral
20.
go back to reference Ranson H, N’Guessan R, Lines J, Moiroux N, Nkuni Z, Corbel V. Pyrethroid resistance in African anopheline mosquitoes: what are the implications for malaria control? Trends Parasitol. 2011;27:91–8.PubMed Ranson H, N’Guessan R, Lines J, Moiroux N, Nkuni Z, Corbel V. Pyrethroid resistance in African anopheline mosquitoes: what are the implications for malaria control? Trends Parasitol. 2011;27:91–8.PubMed
21.
go back to reference Martinez-Torres D, Chandre F, Williamson MS, Darriet F, Bergé JB, Devonshire AL, et al. Molecular characterization of pyrethroid knockdown resistance (kdr) in the major malaria vector Anopheles gambiae s.s. Insect Mol Biol. 1998;7:179–84.PubMed Martinez-Torres D, Chandre F, Williamson MS, Darriet F, Bergé JB, Devonshire AL, et al. Molecular characterization of pyrethroid knockdown resistance (kdr) in the major malaria vector Anopheles gambiae s.s. Insect Mol Biol. 1998;7:179–84.PubMed
22.
go back to reference Ranson H, Jensen B, Vulule JM, Wang X, Hemingway J, Collins FH. Identification of a point mutation in the voltage-gated sodium channel gene of Kenyan Anopheles gambiae associated with resistance to DDT and pyrethroids. Insect Mol Biol. 2000;9:491–7.PubMed Ranson H, Jensen B, Vulule JM, Wang X, Hemingway J, Collins FH. Identification of a point mutation in the voltage-gated sodium channel gene of Kenyan Anopheles gambiae associated with resistance to DDT and pyrethroids. Insect Mol Biol. 2000;9:491–7.PubMed
23.
go back to reference Essandoh J, Yawson AE, Weetman D. Acetylcholinesterase (Ace-1) target site mutation 119S is strongly diagnostic of carbamate and organophosphate resistance in Anopheles gambiae s.s. and Anopheles coluzzii across southern Ghana. Malar J. 2013;12:404.PubMedPubMedCentral Essandoh J, Yawson AE, Weetman D. Acetylcholinesterase (Ace-1) target site mutation 119S is strongly diagnostic of carbamate and organophosphate resistance in Anopheles gambiae s.s. and Anopheles coluzzii across southern Ghana. Malar J. 2013;12:404.PubMedPubMedCentral
24.
go back to reference Djogbenou LS, Pasteur N, Bio-Bangana S, Baldet T, Irish SR, Weill M, et al. Malaria vectors in the Republic of Benin: distribution, of species and molecular forms of the Anopheles gambiae complex. Acta Trop. 2010;114:116–22.PubMed Djogbenou LS, Pasteur N, Bio-Bangana S, Baldet T, Irish SR, Weill M, et al. Malaria vectors in the Republic of Benin: distribution, of species and molecular forms of the Anopheles gambiae complex. Acta Trop. 2010;114:116–22.PubMed
25.
go back to reference Simma EA, Dermauw W, Balabanidou V, Snoeck S, Bryon A, Clark RM, et al. Genome-wide gene expression profiling reveals that cuticle alterations and P450 detoxification are associated with deltamethrin and DDT resistance in Anopheles arabiensis populations from Ethiopia. Pest Manag Sci. 2019;75:1808–18.PubMed Simma EA, Dermauw W, Balabanidou V, Snoeck S, Bryon A, Clark RM, et al. Genome-wide gene expression profiling reveals that cuticle alterations and P450 detoxification are associated with deltamethrin and DDT resistance in Anopheles arabiensis populations from Ethiopia. Pest Manag Sci. 2019;75:1808–18.PubMed
26.
go back to reference Hemingway J, Hawkes NJ, McCarroll L, Ranson H. The molecular basis of insecticide resistance in mosquitoes. Insect Biochem Mol Biol. 2004;34:653–65.PubMed Hemingway J, Hawkes NJ, McCarroll L, Ranson H. The molecular basis of insecticide resistance in mosquitoes. Insect Biochem Mol Biol. 2004;34:653–65.PubMed
27.
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.PubMedPubMedCentral 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.PubMedPubMedCentral
28.
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.PubMedPubMedCentral 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.PubMedPubMedCentral
29.
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. Pestic Biochem Physiol. 2010;96:80–5. 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. Pestic Biochem Physiol. 2010;96:80–5.
30.
go back to reference Owusu-Agyei S, Kasasa S, Gosoniu L, Adjuik M, Anto F, Asoala V, et al. Spatio-temporal malaria transmission patterns in Navrongo demographic surveillance site, northern Ghana. Malar J. 2013;12:63.PubMedPubMedCentral Owusu-Agyei S, Kasasa S, Gosoniu L, Adjuik M, Anto F, Asoala V, et al. Spatio-temporal malaria transmission patterns in Navrongo demographic surveillance site, northern Ghana. Malar J. 2013;12:63.PubMedPubMedCentral
31.
go back to reference Awine T, Malm K, Peprah NY, Silal SP. Spatio-temporal heterogeneity of malaria morbidity in Ghana: analysis of routine health facility data. PLoS ONE. 2018;13:e0191707.PubMedPubMedCentral Awine T, Malm K, Peprah NY, Silal SP. Spatio-temporal heterogeneity of malaria morbidity in Ghana: analysis of routine health facility data. PLoS ONE. 2018;13:e0191707.PubMedPubMedCentral
32.
go back to reference Gogue C, Wagman J, Tynuv K, Saibu A, Yihdego Y, Malm K, et al. An observational analysis of the impact of indoor residual spraying in Northern, Upper East, and Upper West Regions of Ghana: 2014 through 2017. Malar J. 2020;19:242.PubMedPubMedCentral Gogue C, Wagman J, Tynuv K, Saibu A, Yihdego Y, Malm K, et al. An observational analysis of the impact of indoor residual spraying in Northern, Upper East, and Upper West Regions of Ghana: 2014 through 2017. Malar J. 2020;19:242.PubMedPubMedCentral
33.
go back to reference Aregawi M, Malm KL, Wahjib M, Kofi O, Allotey NK, Yaw PN, et al. Effect of anti-malarial interventions on trends of malaria cases, hospital admissions and deaths, 2005–2015, Ghana. Malar J. 2017;16:177.PubMedPubMedCentral Aregawi M, Malm KL, Wahjib M, Kofi O, Allotey NK, Yaw PN, et al. Effect of anti-malarial interventions on trends of malaria cases, hospital admissions and deaths, 2005–2015, Ghana. Malar J. 2017;16:177.PubMedPubMedCentral
34.
go back to reference Afoakwah C, Deng X, Onur I. Malaria infection among children under-five: the use of large-scale interventions in Ghana. BMC Public Health. 2018;18:536.PubMedPubMedCentral Afoakwah C, Deng X, Onur I. Malaria infection among children under-five: the use of large-scale interventions in Ghana. BMC Public Health. 2018;18:536.PubMedPubMedCentral
35.
go back to reference Yawson AE, McCall PJ, Wilson MD, Donnelly MJ. Species abundance and insecticide resistance of Anopheles gambiae in selected areas of Ghana and Burkina Faso. Med Vet Entomol. 2004;18:372–7.PubMed Yawson AE, McCall PJ, Wilson MD, Donnelly MJ. Species abundance and insecticide resistance of Anopheles gambiae in selected areas of Ghana and Burkina Faso. Med Vet Entomol. 2004;18:372–7.PubMed
36.
go back to reference Coleman S, Dadzie SK, Seyoum A, Yihdego Y, Mumba P, Dengela D, et al. A reduction in malaria transmission intensity in Northern Ghana after 7 years of indoor residual spraying. Malar J. 2017;16:324.PubMedPubMedCentral Coleman S, Dadzie SK, Seyoum A, Yihdego Y, Mumba P, Dengela D, et al. A reduction in malaria transmission intensity in Northern Ghana after 7 years of indoor residual spraying. Malar J. 2017;16:324.PubMedPubMedCentral
37.
go back to reference Baffour-Awuah S, Annan AA, Maiga-Ascofare O, Dieudonné SD, Adjei-Kusi P, Owusu-Dabo E, et al. Insecticide resistance in malaria vectors in Kumasi, Ghana. Parasit Vectors. 2016;9:633.PubMedPubMedCentral Baffour-Awuah S, Annan AA, Maiga-Ascofare O, Dieudonné SD, Adjei-Kusi P, Owusu-Dabo E, et al. Insecticide resistance in malaria vectors in Kumasi, Ghana. Parasit Vectors. 2016;9:633.PubMedPubMedCentral
38.
go back to reference Dengela D, Seyoum A, Lucas B, Johns B, George K, Belemvire A, et al. Multi-country assessment of residual bio-efficacy of insecticides used for indoor residual spraying in malaria control on different surface types: results from program monitoring in 17 PMI/USAID-supported IRS countries. Parasit Vectors. 2018;11:71.PubMedPubMedCentral Dengela D, Seyoum A, Lucas B, Johns B, George K, Belemvire A, et al. Multi-country assessment of residual bio-efficacy of insecticides used for indoor residual spraying in malaria control on different surface types: results from program monitoring in 17 PMI/USAID-supported IRS countries. Parasit Vectors. 2018;11:71.PubMedPubMedCentral
39.
go back to reference Ahorlu C, Abuaku B, Amratia P, Oppong S, Valle D, Koram K, et al. Detecting local risk factors for residual malaria in northern Ghana using Bayesian model averaging. Malar J. 2018;17:343.PubMedPubMedCentral Ahorlu C, Abuaku B, Amratia P, Oppong S, Valle D, Koram K, et al. Detecting local risk factors for residual malaria in northern Ghana using Bayesian model averaging. Malar J. 2018;17:343.PubMedPubMedCentral
40.
go back to reference Abuaku B, Ahorlu C, Psychas P, Ricks P, Oppong S, Mensah S, et al. Impact of indoor residual spraying on malaria parasitaemia in the Bunkpurugu-Yunyoo District in northern Ghana. Parasit Vectors. 2018;11:555.PubMedPubMedCentral Abuaku B, Ahorlu C, Psychas P, Ricks P, Oppong S, Mensah S, et al. Impact of indoor residual spraying on malaria parasitaemia in the Bunkpurugu-Yunyoo District in northern Ghana. Parasit Vectors. 2018;11:555.PubMedPubMedCentral
41.
go back to reference Baird JK, Agyei SO, Utz GC, Koram K, Barcus MJ, Jones TR, et al. Seasonal malaria attack rates in infants and young children in northern Ghana. Am J Trop Med Hyg. 2002;66:280–6.PubMed Baird JK, Agyei SO, Utz GC, Koram K, Barcus MJ, Jones TR, et al. Seasonal malaria attack rates in infants and young children in northern Ghana. Am J Trop Med Hyg. 2002;66:280–6.PubMed
42.
go back to reference Vazquez-Prokopec GM, Galvin WA, Kelly R, Kitron U. A new, cost-effective, battery-powered aspirator for adult mosquito collections. J Med Entomol. 2009;46:1256–9.PubMed Vazquez-Prokopec GM, Galvin WA, Kelly R, Kitron U. A new, cost-effective, battery-powered aspirator for adult mosquito collections. J Med Entomol. 2009;46:1256–9.PubMed
43.
go back to reference Muirhead-Thomson RC. A pit shelter for sampling outdoor mosquito populations. Bull World Health Organ. 1958;19:1116–8.PubMedPubMedCentral Muirhead-Thomson RC. A pit shelter for sampling outdoor mosquito populations. Bull World Health Organ. 1958;19:1116–8.PubMedPubMedCentral
44.
go back to reference Gillies MT, Coetzee M. A Supplement to the Anophelinae of the South of the Sahara (Afrotropical Region). South African Inst Med Res. 1987;55:1–143. Gillies MT, Coetzee M. A Supplement to the Anophelinae of the South of the Sahara (Afrotropical Region). South African Inst Med Res. 1987;55:1–143.
45.
go back to reference WHO. Test procedures for insecticide resistance monitoring in malaria vector mosquitoes. 2nd ed. Geneva: World Health Organization; 2016. WHO. Test procedures for insecticide resistance monitoring in malaria vector mosquitoes. 2nd ed. Geneva: World Health Organization; 2016.
46.
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
47.
go back to reference Favia G, Lanfrancotti A, Spanos L, Sidén-Kiamos I, Louis C. Molecular characterization of ribosomal DNA polymorphisms discriminating among chromosomal forms of Anopheles gambiae s.s.. Insect Mol Biol. 2001;10:19–23.PubMed Favia G, Lanfrancotti A, Spanos L, Sidén-Kiamos I, Louis C. Molecular characterization of ribosomal DNA polymorphisms discriminating among chromosomal forms of Anopheles gambiae s.s.. Insect Mol Biol. 2001;10:19–23.PubMed
48.
go back to reference Hunt RH, Fuseini G, Knowles S, Stiles-Ocran J, Verster R, Kaiser ML, et al. Insecticide resistance in malaria vector mosquitoes at four localities in Ghana, West Africa. Parasit Vectors. 2011;4:107.PubMedPubMedCentral Hunt RH, Fuseini G, Knowles S, Stiles-Ocran J, Verster R, Kaiser ML, et al. Insecticide resistance in malaria vector mosquitoes at four localities in Ghana, West Africa. Parasit Vectors. 2011;4:107.PubMedPubMedCentral
49.
go back to reference Bass C, Nikou D, Donnelly MJ, Williamson MS, Ranson H, Ball A, et al. Detection of knockdown resistance (kdr) mutations in Anopheles gambiae: a comparison of two new high-throughput assays with existing methods. Malar J. 2007;6:111.PubMedPubMedCentral Bass C, Nikou D, Donnelly MJ, Williamson MS, Ranson H, Ball A, et al. Detection of knockdown resistance (kdr) mutations in Anopheles gambiae: a comparison of two new high-throughput assays with existing methods. Malar J. 2007;6:111.PubMedPubMedCentral
50.
go back to reference Brogdon WG, Beach RF, Stewart JM, Castanaza L. Microplate assay analysis of the distribution of organophosphate and carbamate resistance in Guatemalan Anopheles albimanus. Bull World Health Organ. 1988;66:339–46.PubMedPubMedCentral Brogdon WG, Beach RF, Stewart JM, Castanaza L. Microplate assay analysis of the distribution of organophosphate and carbamate resistance in Guatemalan Anopheles albimanus. Bull World Health Organ. 1988;66:339–46.PubMedPubMedCentral
51.
go back to reference Kent RJ, Norris DE. Identification of mammalian blood meals in mosquitoes by a multiplexed polymerase chain reaction targeting cytochrome B. Am J Trop Med Hyg. 2005;73:336–42.PubMed Kent RJ, Norris DE. Identification of mammalian blood meals in mosquitoes by a multiplexed polymerase chain reaction targeting cytochrome B. Am J Trop Med Hyg. 2005;73:336–42.PubMed
52.
go back to reference Kabula B, Kisinza W, Tungu P, Ndege C, Batengana B, Kollo D, et al. Co-occurrence and distribution of East (L1014S) and West (L1014F) African knock-down resistance in Anopheles gambiae sensu lato population of Tanzania. Trop Med Int Health. 2014;19:331–41.PubMed Kabula B, Kisinza W, Tungu P, Ndege C, Batengana B, Kollo D, et al. Co-occurrence and distribution of East (L1014S) and West (L1014F) African knock-down resistance in Anopheles gambiae sensu lato population of Tanzania. Trop Med Int Health. 2014;19:331–41.PubMed
53.
go back to reference Mitchell SN, Stevenson BJ, Muller P, Wilding CS, Egyir-Yawson A, Field SG, et al. Identification and validation of a gene causing cross-resistance between insecticide classes in Anopheles gambiae from Ghana. Proc Natl Acad Sci USA. 2012;109:6147–52.PubMedPubMedCentral Mitchell SN, Stevenson BJ, Muller P, Wilding CS, Egyir-Yawson A, Field SG, et al. Identification and validation of a gene causing cross-resistance between insecticide classes in Anopheles gambiae from Ghana. Proc Natl Acad Sci USA. 2012;109:6147–52.PubMedPubMedCentral
54.
go back to reference Reid MC, McKenzie FE. The contribution of agricultural insecticide use to increasing insecticide resistance in African malaria vectors. Malar J. 2016;15:107.PubMedPubMedCentral Reid MC, McKenzie FE. The contribution of agricultural insecticide use to increasing insecticide resistance in African malaria vectors. Malar J. 2016;15:107.PubMedPubMedCentral
55.
go back to reference NPASP (Northern Presbyterian Agricultural Service and Partners). Ghana’s pesticide crisis: a need for further government action. 2012. NPASP (Northern Presbyterian Agricultural Service and Partners). Ghana’s pesticide crisis: a need for further government action. 2012.
56.
go back to reference Dadzie SK, Chabi J, Asafu-Adjaye A, Owusu-Akrofi O, Baffoe-Wilmot A, Malm K, et al. Evaluation of piperonyl butoxide in enhancing the efficacy of pyrethroid insecticides against resistant Anopheles gambiae s.l. in Ghana. Malar J. 2017;16:342.PubMedPubMedCentral Dadzie SK, Chabi J, Asafu-Adjaye A, Owusu-Akrofi O, Baffoe-Wilmot A, Malm K, et al. Evaluation of piperonyl butoxide in enhancing the efficacy of pyrethroid insecticides against resistant Anopheles gambiae s.l. in Ghana. Malar J. 2017;16:342.PubMedPubMedCentral
57.
go back to reference Djègbè I, Akoton R, Tchigossou G, Ahadji-Dabla KM, Atoyebi SM, Adéoti R, et al. First report of the presence of L1014S Knockdown-resistance mutation in Anopheles gambiae s.s. and Anopheles coluzzii from Togo. West Africa. Wellcome Open Res. 2018;3:30.PubMed Djègbè I, Akoton R, Tchigossou G, Ahadji-Dabla KM, Atoyebi SM, Adéoti R, et al. First report of the presence of L1014S Knockdown-resistance mutation in Anopheles gambiae s.s. and Anopheles coluzzii from Togo. West Africa. Wellcome Open Res. 2018;3:30.PubMed
58.
go back to reference Donnelly MJ, Corbel V, Weetman D, Wilding CS, Williamson MS, Black WC IV. Does kdr genotype predict insecticide-resistance phenotype in mosquitoes? Trends Parasitol. 2009;25:213–9.PubMed Donnelly MJ, Corbel V, Weetman D, Wilding CS, Williamson MS, Black WC IV. Does kdr genotype predict insecticide-resistance phenotype in mosquitoes? Trends Parasitol. 2009;25:213–9.PubMed
59.
go back to reference Liu N. Insecticide resistance in mosquitoes: impact, mechanisms, and research directions. Annu Rev Entomol. 2015;60:537–59.PubMed Liu N. Insecticide resistance in mosquitoes: impact, mechanisms, and research directions. Annu Rev Entomol. 2015;60:537–59.PubMed
60.
go back to reference Ochomo E, Bayoh MN, Brogdon WG, Gimnig JE, Ouma C, Vulule JM, et al. Pyrethroid resistance in Anopheles gambiae ss and Anopheles arabiensis in western Kenya: Phenotypic, metabolic and target site characterizations of three populations. Med Vet Entomol. 2013;27:156–64.PubMed Ochomo E, Bayoh MN, Brogdon WG, Gimnig JE, Ouma C, Vulule JM, et al. Pyrethroid resistance in Anopheles gambiae ss and Anopheles arabiensis in western Kenya: Phenotypic, metabolic and target site characterizations of three populations. Med Vet Entomol. 2013;27:156–64.PubMed
61.
go back to reference Matowo J, Kulkarni MA, Mosha FW, Oxborough RM, Kitau JA, Tenu F, et al. Biochemical basis of permethrin resistance in Anopheles arabiensis from Lower Moshi, north-eastern Tanzania. Malar J. 2010;9:193.PubMedPubMedCentral Matowo J, Kulkarni MA, Mosha FW, Oxborough RM, Kitau JA, Tenu F, et al. Biochemical basis of permethrin resistance in Anopheles arabiensis from Lower Moshi, north-eastern Tanzania. Malar J. 2010;9:193.PubMedPubMedCentral
62.
go back to reference Machani MG, Ochomo E, Sang D, Bonizzoni M, Zhou G, Githeko AK, et al. Influence of blood meal and age of mosquitoes on susceptibility to pyrethroids in Anopheles gambiae from Western Kenya. Malar J. 2019;18:112.PubMedPubMedCentral Machani MG, Ochomo E, Sang D, Bonizzoni M, Zhou G, Githeko AK, et al. Influence of blood meal and age of mosquitoes on susceptibility to pyrethroids in Anopheles gambiae from Western Kenya. Malar J. 2019;18:112.PubMedPubMedCentral
63.
go back to reference Collins E, Vaselli NM, Sylla M, Beavogui AH, Orsborne J, Lawrence G, et al. The relationship between insecticide resistance, mosquito age and malaria prevalence in Anopheles gambiae s.l. from Guinea. Sci Rep. 2019;9:8846.PubMedPubMedCentral Collins E, Vaselli NM, Sylla M, Beavogui AH, Orsborne J, Lawrence G, et al. The relationship between insecticide resistance, mosquito age and malaria prevalence in Anopheles gambiae s.l. from Guinea. Sci Rep. 2019;9:8846.PubMedPubMedCentral
64.
go back to reference Garrett-Jones C, Boreham PFL, Pant CP. Feeding habits of anophelines (Diptera: culicidae) in 1971–78, with reference to the human blood index: a review. Bull Entomol Res. 1980;70:165–85. Garrett-Jones C, Boreham PFL, Pant CP. Feeding habits of anophelines (Diptera: culicidae) in 1971–78, with reference to the human blood index: a review. Bull Entomol Res. 1980;70:165–85.
65.
go back to reference Stevenson JC, Simubali L, Mbambara S, Musonda M, Mweetwa S, Mudenda T, et al. Detection of Plasmodium falciparum infection in Anopheles squamosus (Diptera: culicidae) in an area targeted for malaria elimination, Southern Zambia. J Med Entomol. 2016;53:1482–7.PubMedPubMedCentral Stevenson JC, Simubali L, Mbambara S, Musonda M, Mweetwa S, Mudenda T, et al. Detection of Plasmodium falciparum infection in Anopheles squamosus (Diptera: culicidae) in an area targeted for malaria elimination, Southern Zambia. J Med Entomol. 2016;53:1482–7.PubMedPubMedCentral
66.
go back to reference Mayagaya VS, Nkwengulila G, Lyimo IN, Kihonda J, Mtambala H, Ngonyani H, et al. The impact of livestock on the abundance, resting behaviour and sporozoite rate of malaria vectors in southern Tanzania. Malar J. 2015;14:17.PubMedPubMedCentral Mayagaya VS, Nkwengulila G, Lyimo IN, Kihonda J, Mtambala H, Ngonyani H, et al. The impact of livestock on the abundance, resting behaviour and sporozoite rate of malaria vectors in southern Tanzania. Malar J. 2015;14:17.PubMedPubMedCentral
Metadata
Title
Insecticide resistance in indoor and outdoor-resting Anopheles gambiae in Northern Ghana
Authors
Majidah Hamid-Adiamoh
Alfred Amambua-Ngwa
Davis Nwakanma
Umberto D’Alessandro
Gordon A. Awandare
Yaw A. Afrane
Publication date
01-12-2020
Publisher
BioMed Central
Keyword
Malaria
Published in
Malaria Journal / Issue 1/2020
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-020-03388-1

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