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Published in: Malaria Journal 1/2020

Open Access 01-12-2020 | Malaria | Research

Preferred resting surfaces of dominant malaria vectors inside different house types in rural south-eastern Tanzania

Authors: Betwel J. Msugupakulya, Emmanuel W. Kaindoa, Halfan S. Ngowo, Japhet M. Kihonda, Najat F. Kahamba, Dickson S. Msaky, Damaris Matoke-Muhia, Patrick K. Tungu, Fredros O. Okumu

Published in: Malaria Journal | Issue 1/2020

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Abstract

Background

Malaria control in Africa relies extensively on indoor residual spraying (IRS) and insecticide-treated nets (ITNs). IRS typically targets mosquitoes resting on walls, and in few cases, roofs and ceilings, using contact insecticides. Unfortunately, little attention is paid to where malaria vectors actually rest indoors, and how such knowledge could be used to improve IRS. This study investigated preferred resting surfaces of two major malaria vectors, Anopheles funestus and Anopheles arabiensis, inside four common house types in rural south-eastern Tanzania.

Methods

The assessment was done inside 80 houses including: 20 with thatched roofs and mud walls, 20 with thatched roofs and un-plastered brick walls, 20 with metal roofs and un-plastered brick walls, and 20 with metal roofs and plastered brick walls, across four villages. In each house, resting mosquitoes were sampled in mornings (6 a.m.–8 a.m.), evenings (6 p.m.–8 p.m.) and at night (11 p.m.–12.00 a.m.) using Prokopack aspirators from multiple surfaces (walls, undersides of roofs, floors, furniture, utensils, clothing, curtains and bed nets).

Results

Overall, only 26% of An. funestus and 18% of An. arabiensis were found on walls. In grass-thatched houses, 33–55% of An. funestus and 43–50% of An. arabiensis rested under roofs, while in metal-roofed houses, only 16–20% of An. funestus and 8–30% of An. arabiensis rested under roofs. Considering all data together, approximately 40% of mosquitoes rested on surfaces not typically targeted by IRS, i.e. floors, furniture, utensils, clothing and bed nets. These proportions were particularly high in metal-roofed houses (47–53% of An. funestus; 60–66% of An. arabiensis).

Conclusion

While IRS typically uses contact insecticides to target adult mosquitoes on walls, and occasionally roofs and ceilings, significant proportions of vectors rest on surfaces not usually sprayed. This gap exceeds one-third of malaria mosquitoes in grass-thatched houses, and can reach two-thirds in metal-roofed houses. Where field operations exclude roofs during IRS, the gaps can be much greater. In conclusion, there is need for locally-obtained data on mosquito resting behaviours and how these influence the overall impact and costs of IRS. This study also emphasizes the need for alternative approaches, e.g. house screening, which broadly tackle mosquitoes beyond areas reachable by IRS and ITNs.
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Literature
1.
go back to reference WHO. World malaria report. Geneva: World Health Organization; 2018. WHO. World malaria report. Geneva: World Health Organization; 2018.
2.
go back to reference Bhatt S, Weiss DJ, Cameron E, Bisanzio D, Mappin B, Dalrymple U, et al. The effect of malaria control on Plasmodium falciparum in Africa between 2000 and 2015. Nature. 2015;526:207–11.PubMedPubMedCentralCrossRef Bhatt S, Weiss DJ, Cameron E, Bisanzio D, Mappin B, Dalrymple U, et al. The effect of malaria control on Plasmodium falciparum in Africa between 2000 and 2015. Nature. 2015;526:207–11.PubMedPubMedCentralCrossRef
3.
go back to reference Mashauri FM, Kinung’hi SM, Kaatano GM, Magesa SM, Kishamawe C, Mwanga JR, et al. Impact of indoor residual spraying of lambda-cyhalothrin on malaria prevalence and anemia in an epidemic-prone district of Muleba, North-Western Tanzania. Am J Trop Med Hyg. 2013;88:841–9.PubMedPubMedCentralCrossRef Mashauri FM, Kinung’hi SM, Kaatano GM, Magesa SM, Kishamawe C, Mwanga JR, et al. Impact of indoor residual spraying of lambda-cyhalothrin on malaria prevalence and anemia in an epidemic-prone district of Muleba, North-Western Tanzania. Am J Trop Med Hyg. 2013;88:841–9.PubMedPubMedCentralCrossRef
4.
go back to reference Bhattarai A, Ali AS, Kachur SP, Mårtensson A, Abbas AK, Khatib R, et al. Impact of artemisinin-based combination therapy and insecticide-treated nets on malaria burden in Zanzibar. PLoS Med. 2007;4:1784–90.CrossRef Bhattarai A, Ali AS, Kachur SP, Mårtensson A, Abbas AK, Khatib R, et al. Impact of artemisinin-based combination therapy and insecticide-treated nets on malaria burden in Zanzibar. PLoS Med. 2007;4:1784–90.CrossRef
5.
go back to reference Selemani M, Msengwa AS, Mrema S, Shamte A, Mahande MJ, Yeates K, et al. Assessing the effects of mosquito nets on malaria mortality using a space time model: a case study of Rufiji and Ifakara Health and Demographic Surveillance System sites in rural Tanzania. Malar J. 2016;15:257.PubMedPubMedCentralCrossRef Selemani M, Msengwa AS, Mrema S, Shamte A, Mahande MJ, Yeates K, et al. Assessing the effects of mosquito nets on malaria mortality using a space time model: a case study of Rufiji and Ifakara Health and Demographic Surveillance System sites in rural Tanzania. Malar J. 2016;15:257.PubMedPubMedCentralCrossRef
6.
go back to reference Alba S, Nathan R, Schulze A, Mshinda H, Lengeler C. Child mortality patterns in rural Tanzania: an observational study on the impact of malaria control interventions. Int J Epidemiol. 2014;43:204–15.PubMedCrossRef Alba S, Nathan R, Schulze A, Mshinda H, Lengeler C. Child mortality patterns in rural Tanzania: an observational study on the impact of malaria control interventions. Int J Epidemiol. 2014;43:204–15.PubMedCrossRef
7.
go back to reference National Bureau of Statistics (NBS), Office of the Chief Government Statistician (OCGS), Ministry of Health, Community Development, Gender, Elderly and Children (MOHCDGEC) [Tanzania Mainland], Ministry of Health (MOH) [Zanzibar], ICF. Tanzania Malaria Indicator Survey. Dar es Salaam, Tanzania, and Rockville, Maryland: MoHCDGEC, MoH, NBS, OCGS, ICF; 2018. National Bureau of Statistics (NBS), Office of the Chief Government Statistician (OCGS), Ministry of Health, Community Development, Gender, Elderly and Children (MOHCDGEC) [Tanzania Mainland], Ministry of Health (MOH) [Zanzibar], ICF. Tanzania Malaria Indicator Survey. Dar es Salaam, Tanzania, and Rockville, Maryland: MoHCDGEC, MoH, NBS, OCGS, ICF; 2018.
8.
go back to reference WHO. Global technical strategy for malaria 2016–2030. Geneva: World Health Organization; 2015. WHO. Global technical strategy for malaria 2016–2030. Geneva: World Health Organization; 2015.
9.
go back to reference WHO. High burden to high impact: a targeted malaria response. Geneva: World Health Organization; 2018. WHO. High burden to high impact: a targeted malaria response. Geneva: World Health Organization; 2018.
10.
go back to reference Hemingway J, Ranson H, Magill A, Kolaczinski J, Fornadel C, Gimnig J, et al. Averting a malaria disaster: will insecticide resistance derail malaria control? Lancet. 2016;387:1785–8.PubMedPubMedCentralCrossRef Hemingway J, Ranson H, Magill A, Kolaczinski J, Fornadel C, Gimnig J, et al. Averting a malaria disaster: will insecticide resistance derail malaria control? Lancet. 2016;387:1785–8.PubMedPubMedCentralCrossRef
11.
go back to reference Ranson H, Lissenden N. Insecticide resistance in African Anopheles mosquitoes: a worsening situation that needs urgent action to maintain malaria control. Trends Parasitol. 2016;32:187–96.CrossRefPubMed Ranson H, Lissenden N. Insecticide resistance in African Anopheles mosquitoes: a worsening situation that needs urgent action to maintain malaria control. Trends Parasitol. 2016;32:187–96.CrossRefPubMed
12.
go back to reference Sherrard-Smith E, Skarp JE, Beale AD, Fornadel C, Norris LC, Moore SJ. Mosquito feeding behavior and how it influences residual malaria transmission across Africa. Proc Natl Acad Sci USA. 2019;116:15086–95.PubMedCrossRefPubMedCentral Sherrard-Smith E, Skarp JE, Beale AD, Fornadel C, Norris LC, Moore SJ. Mosquito feeding behavior and how it influences residual malaria transmission across Africa. Proc Natl Acad Sci USA. 2019;116:15086–95.PubMedCrossRefPubMedCentral
13.
go back to reference Monroe A, Moore S, Koenker H, Lynch M, Ricotta E. Measuring and characterizing night time human behaviour as it relates to residual malaria transmission in sub-Saharan Africa: a review of the published literature. Malar J. 2019;18:6.PubMedPubMedCentralCrossRef Monroe A, Moore S, Koenker H, Lynch M, Ricotta E. Measuring and characterizing night time human behaviour as it relates to residual malaria transmission in sub-Saharan Africa: a review of the published literature. Malar J. 2019;18:6.PubMedPubMedCentralCrossRef
14.
go back to reference Finda MF, Moshi IR, Monroe A, Limwagu AJ, Nyoni P, Swai JK, et al. Linking human behaviours and malaria vector biting risk in south-eastern Tanzania. PLoS ONE. 2019;14:e0217414.PubMedPubMedCentralCrossRef Finda MF, Moshi IR, Monroe A, Limwagu AJ, Nyoni P, Swai JK, et al. Linking human behaviours and malaria vector biting risk in south-eastern Tanzania. PLoS ONE. 2019;14:e0217414.PubMedPubMedCentralCrossRef
15.
go back to reference Nkya TE, Poupardin R, Laporte F, Akhouayri I, Mosha F, Magesa S, et al. Impact of agriculture on the selection of insecticide resistance in the malaria vector Anopheles gambiae: a multigenerational study in controlled cinditions. Parasit Vectors. 2014;7:480.PubMedPubMedCentral Nkya TE, Poupardin R, Laporte F, Akhouayri I, Mosha F, Magesa S, et al. Impact of agriculture on the selection of insecticide resistance in the malaria vector Anopheles gambiae: a multigenerational study in controlled cinditions. Parasit Vectors. 2014;7:480.PubMedPubMedCentral
16.
go back to reference Protopopoff N, Verhaeghen K, Van Bortel W, Roelants P, Marcotty T, Baza D, et al. A significant increase in kdr in Anopheles gambiae is associated with an intensive vector control intervention in Burundi highlands. Trop Med Int Health. 2008;13:1479–87.PubMedCrossRef Protopopoff N, Verhaeghen K, Van Bortel W, Roelants P, Marcotty T, Baza D, et al. A significant increase in kdr in Anopheles gambiae is associated with an intensive vector control intervention in Burundi highlands. Trop Med Int Health. 2008;13:1479–87.PubMedCrossRef
17.
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.PubMedCrossRef 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.PubMedCrossRef
18.
go back to reference Killeen GF, Chitnis N. Potential causes and consequences of behavioural resilience and resistance in malaria vector populations: a mathematical modelling analysis. Malar J. 2014;13:97.PubMedPubMedCentralCrossRef Killeen GF, Chitnis N. Potential causes and consequences of behavioural resilience and resistance in malaria vector populations: a mathematical modelling analysis. Malar J. 2014;13:97.PubMedPubMedCentralCrossRef
19.
go back to reference Russell TL, Lwetoijera DW, Maliti D, Chipwaza B, Kihonda J, Charlwood JD, et al. Impact of promoting longer-lasting insecticide treatment of bed nets upon malaria transmission in a rural Tanzanian setting with pre-existing high coverage of untreated nets. Malar J. 2010;9:187.PubMedPubMedCentralCrossRef Russell TL, Lwetoijera DW, Maliti D, Chipwaza B, Kihonda J, Charlwood JD, et al. Impact of promoting longer-lasting insecticide treatment of bed nets upon malaria transmission in a rural Tanzanian setting with pre-existing high coverage of untreated nets. Malar J. 2010;9:187.PubMedPubMedCentralCrossRef
20.
go back to reference Moiroux N, Gomez MB, Pennetier C, Elanga E, Djènontin A, Chandre F, et al. Changes in Anopheles funestus biting behavior following universal coverage of long-lasting insecticidal nets in Benin. J Infect Dis. 2012;206:1622–9.PubMedCrossRef Moiroux N, Gomez MB, Pennetier C, Elanga E, Djènontin A, Chandre F, et al. Changes in Anopheles funestus biting behavior following universal coverage of long-lasting insecticidal nets in Benin. J Infect Dis. 2012;206:1622–9.PubMedCrossRef
21.
go back to reference Kouznetsov RL. Malaria control by application of indoor spraying of residual insecticides in tropical Africa and its impact on community health. Trop Doct. 1977;7:81–91.PubMedCrossRef Kouznetsov RL. Malaria control by application of indoor spraying of residual insecticides in tropical Africa and its impact on community health. Trop Doct. 1977;7:81–91.PubMedCrossRef
22.
go back to reference Nájera JA, González-Silva M, Alonso PL. Some lessons for the future from the global malaria eradication programme (1955–1969). PLoS Med. 2011;8:e1000412.PubMedPubMedCentralCrossRef Nájera JA, González-Silva M, Alonso PL. Some lessons for the future from the global malaria eradication programme (1955–1969). PLoS Med. 2011;8:e1000412.PubMedPubMedCentralCrossRef
23.
go back to reference WHO. An operational manual for indoor residual spraying (IRS) for malaria transmission control and elimination. Geneva: World Health Organization; 2015. WHO. An operational manual for indoor residual spraying (IRS) for malaria transmission control and elimination. Geneva: World Health Organization; 2015.
24.
go back to reference Pringle G. Malaria in the pare area of Tanzania III The course of malaria transmission since the suspension of an experimental programme of residual insecticide spraying. Trans R Soc Trop Med Hyg. 1967;61:69–79.PubMedCrossRef Pringle G. Malaria in the pare area of Tanzania III The course of malaria transmission since the suspension of an experimental programme of residual insecticide spraying. Trans R Soc Trop Med Hyg. 1967;61:69–79.PubMedCrossRef
25.
go back to reference The PMI VectorLink Project. 2018/2019 Tanzania End of Spray Report. MD: Rockville; 2019. The PMI VectorLink Project. 2018/2019 Tanzania End of Spray Report. MD: Rockville; 2019.
26.
go back to reference National Malaria Control Programme. National malaria strategic plan 2014–2020. Dar es Salaam; 2014. National Malaria Control Programme. National malaria strategic plan 2014–2020. Dar es Salaam; 2014.
27.
go back to reference U.S. President’s Malaria Initiative. PMI 13th annual report to congress. Washington; 2019. U.S. President’s Malaria Initiative. PMI 13th annual report to congress. Washington; 2019.
29.
go back to reference WHO. Global plan for insecticide resistance management in malaria vectors. Geneva: World Health Organization; 2012. WHO. Global plan for insecticide resistance management in malaria vectors. Geneva: World Health Organization; 2012.
31.
go back to reference Protopopoff N, Mosha JF, Lukole E, Charlwood JD, Wright A, Mwalimu CD, et al. Effectiveness of a long-lasting piperonyl butoxide-treated insecticidal net and indoor residual spray interventions, separately and together, against malaria transmitted by pyrethroid-resistant mosquitoes: a cluster, randomised controlled, two-by-two fact. Lancet. 2018;391:1577–88.PubMedPubMedCentralCrossRef Protopopoff N, Mosha JF, Lukole E, Charlwood JD, Wright A, Mwalimu CD, et al. Effectiveness of a long-lasting piperonyl butoxide-treated insecticidal net and indoor residual spray interventions, separately and together, against malaria transmitted by pyrethroid-resistant mosquitoes: a cluster, randomised controlled, two-by-two fact. Lancet. 2018;391:1577–88.PubMedPubMedCentralCrossRef
32.
go back to reference Tiono AB, Ouédraogo A, Ouattara D, Bougouma EC, Coulibaly S, Diarra A, et al. Efficacy of Olyset Duo, a bednet containing pyriproxyfen and permethrin, versus a permethrin-only net against clinical malaria in an area with highly pyrethroid-resistant vectors in rural Burkina Faso: a cluster-randomised controlled trial. Lancet. 2018;392:569–80.PubMedCrossRef Tiono AB, Ouédraogo A, Ouattara D, Bougouma EC, Coulibaly S, Diarra A, et al. Efficacy of Olyset Duo, a bednet containing pyriproxyfen and permethrin, versus a permethrin-only net against clinical malaria in an area with highly pyrethroid-resistant vectors in rural Burkina Faso: a cluster-randomised controlled trial. Lancet. 2018;392:569–80.PubMedCrossRef
33.
go back to reference Gleave K, Lissenden N, Richardson M, Choi L, Ranson H. Piperonyl butoxide (PBO) combined with pyrethroids in insecticide-treated nets to prevent malaria in Africa. Cochrane Database Syst Rev. 2018;11:CD012776.PubMed Gleave K, Lissenden N, Richardson M, Choi L, Ranson H. Piperonyl butoxide (PBO) combined with pyrethroids in insecticide-treated nets to prevent malaria in Africa. Cochrane Database Syst Rev. 2018;11:CD012776.PubMed
34.
go back to reference Tusting LS, Bisanzio D, Alabaster G, Cameron E, Cibulskis R, Davies M, et al. Mapping changes in housing in sub-Saharan Africa from 2000 to 2015. Nature. 2019;568:391–4.PubMedPubMedCentralCrossRef Tusting LS, Bisanzio D, Alabaster G, Cameron E, Cibulskis R, Davies M, et al. Mapping changes in housing in sub-Saharan Africa from 2000 to 2015. Nature. 2019;568:391–4.PubMedPubMedCentralCrossRef
35.
go back to reference Tusting LS, Bottomley C, Gibson H, Kleinschmidt I, Tatem AJ, Lindsay SW, et al. Housing improvements and malaria risk in sub-Saharan Africa: a multi-country analysis of survey data. PLoS Med. 2017;14:e1002234.PubMedPubMedCentralCrossRef Tusting LS, Bottomley C, Gibson H, Kleinschmidt I, Tatem AJ, Lindsay SW, et al. Housing improvements and malaria risk in sub-Saharan Africa: a multi-country analysis of survey data. PLoS Med. 2017;14:e1002234.PubMedPubMedCentralCrossRef
36.
go back to reference Tusting LS, Ippolito MM, Willey BA, Kleinschmidt I, Dorsey G, Gosling RD, et al. The evidence for improving housing to reduce malaria: a systematic review and meta-analysis. Malar J. 2015;14:209.PubMedPubMedCentralCrossRef Tusting LS, Ippolito MM, Willey BA, Kleinschmidt I, Dorsey G, Gosling RD, et al. The evidence for improving housing to reduce malaria: a systematic review and meta-analysis. Malar J. 2015;14:209.PubMedPubMedCentralCrossRef
37.
go back to reference Kirby MJ, Ameh D, Green C, Jawara M, Milligan PJ, Snell PC, et al. Efficacy of two different house screening interventions against exposure to malaria and anaemia in children in The Gambia: a randomized controlled trial. Lancet. 2013;374:998–1009.CrossRef Kirby MJ, Ameh D, Green C, Jawara M, Milligan PJ, Snell PC, et al. Efficacy of two different house screening interventions against exposure to malaria and anaemia in children in The Gambia: a randomized controlled trial. Lancet. 2013;374:998–1009.CrossRef
38.
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.PubMedCrossRef 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.PubMedCrossRef
39.
go back to reference Smith A. The preferential indoor resting habits of Anopheles gambiae in the Umbugwe area of Tanganyika. East Afr Med J. 1962;39:631–5.PubMed Smith A. The preferential indoor resting habits of Anopheles gambiae in the Umbugwe area of Tanganyika. East Afr Med J. 1962;39:631–5.PubMed
40.
go back to reference Smith A. Studies on domestic habits of Anopheles gambiae that affect its vulnerability to insecticides. East Afr Med J. 1962;39:15–24.PubMed Smith A. Studies on domestic habits of Anopheles gambiae that affect its vulnerability to insecticides. East Afr Med J. 1962;39:15–24.PubMed
41.
go back to reference Lindsay SW, Jawara M, Mwesigwa J, Achan J, Bayoh N, Bradley J, et al. Reduced mosquito survival in metal-roof houses may contribute to a decline in malaria transmission in sub-Saharan Africa. Sci Rep. 2019;9:7770.PubMedPubMedCentralCrossRef Lindsay SW, Jawara M, Mwesigwa J, Achan J, Bayoh N, Bradley J, et al. Reduced mosquito survival in metal-roof houses may contribute to a decline in malaria transmission in sub-Saharan Africa. Sci Rep. 2019;9:7770.PubMedPubMedCentralCrossRef
42.
go back to reference Okech BA, Gouagna LC, Knols BGJ, Kabiru EW, Killeen GF, Beier JC, et al. Influence of indoor microclimate and diet on survival of Anopheles gambiae s.s. (Diptera: Culicidae) in village house conditions in western Kenya. Int J Trop Insect Sci. 2004;24:207–12.CrossRef Okech BA, Gouagna LC, Knols BGJ, Kabiru EW, Killeen GF, Beier JC, et al. Influence of indoor microclimate and diet on survival of Anopheles gambiae s.s. (Diptera: Culicidae) in village house conditions in western Kenya. Int J Trop Insect Sci. 2004;24:207–12.CrossRef
43.
go back to reference Lwetoijera DW, Harris C, Kiware SS, Dongus S, Devine GJ, McCall PJ, et al. Increasing role of Anopheles funestus and Anopheles arabiensis in malaria transmission in the Kilombero Valley, Tanzania. Malar J. 2014;13:331.PubMedPubMedCentralCrossRef Lwetoijera DW, Harris C, Kiware SS, Dongus S, Devine GJ, McCall PJ, et al. Increasing role of Anopheles funestus and Anopheles arabiensis in malaria transmission in the Kilombero Valley, Tanzania. Malar J. 2014;13:331.PubMedPubMedCentralCrossRef
44.
go back to reference Kaindoa EW, Matowo NS, Ngowo HS, Mkandawile G, Mmbando A, Finda M, et al. Interventions that effectively target Anopheles funestus mosquitoes could significantly improve control of persistent malaria transmission in south–eastern Tanzania. PLoS ONE. 2017;12:e0177807.PubMedPubMedCentralCrossRef Kaindoa EW, Matowo NS, Ngowo HS, Mkandawile G, Mmbando A, Finda M, et al. Interventions that effectively target Anopheles funestus mosquitoes could significantly improve control of persistent malaria transmission in south–eastern Tanzania. PLoS ONE. 2017;12:e0177807.PubMedPubMedCentralCrossRef
46.
go back to reference Matowo NS, Abbasi S, Munhenga G, Tanner M, Mapua SA, Oullo D, et al. Fine-scale spatial and temporal variations in insecticide resistance in Culex pipiens complex mosquitoes in rural south-eastern Tanzania. Parasit Vectors. 2019;12:413.PubMedPubMedCentralCrossRef Matowo NS, Abbasi S, Munhenga G, Tanner M, Mapua SA, Oullo D, et al. Fine-scale spatial and temporal variations in insecticide resistance in Culex pipiens complex mosquitoes in rural south-eastern Tanzania. Parasit Vectors. 2019;12:413.PubMedPubMedCentralCrossRef
47.
go back to reference Maia MF, Robinson A, John A, Mgando J, Simfukwe E, Moore SJ. Comparison of the CDC Backpack aspirator and the Prokopack aspirator for sampling indoor- and outdoor-resting mosquitoes in southern Tanzania. Parasit Vectors. 2011;4:124.PubMedPubMedCentralCrossRef Maia MF, Robinson A, John A, Mgando J, Simfukwe E, Moore SJ. Comparison of the CDC Backpack aspirator and the Prokopack aspirator for sampling indoor- and outdoor-resting mosquitoes in southern Tanzania. Parasit Vectors. 2011;4:124.PubMedPubMedCentralCrossRef
48.
go back to reference Gillies MT, Coetzee M. A supplement to the Anophelinae of Africa south of the Sahara (Afrotropical Region). Johannesburg: South African Medical Research Institute; 1987. Gillies MT, Coetzee M. A supplement to the Anophelinae of Africa south of the Sahara (Afrotropical Region). Johannesburg: South African Medical Research Institute; 1987.
49.
go back to reference Koekemoer LL, Kamau L, Hunt RH, Coetzee M. A cocktail polymerase chain reaction assay to identify members of the Anopheles funestus (Diptera: Culicidae) group. Am J Trop Med Hyg. 2002;66:804–11.PubMedCrossRef Koekemoer LL, Kamau L, Hunt RH, Coetzee M. A cocktail polymerase chain reaction assay to identify members of the Anopheles funestus (Diptera: Culicidae) group. Am J Trop Med Hyg. 2002;66:804–11.PubMedCrossRef
50.
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.PubMedCrossRef 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.PubMedCrossRef
51.
go back to reference Beier JC, Perkins PV, Wirtz RA, Koros J, Diggs D, Gargan TP, et al. Bloodmeal identification by direct enzyme-linked immunosorbent assay (ELISA), tested on Anopheles (Diptera: Culicidae) in Kenya. J Med Entomol. 1988;25:9–16.PubMedCrossRef Beier JC, Perkins PV, Wirtz RA, Koros J, Diggs D, Gargan TP, et al. Bloodmeal identification by direct enzyme-linked immunosorbent assay (ELISA), tested on Anopheles (Diptera: Culicidae) in Kenya. J Med Entomol. 1988;25:9–16.PubMedCrossRef
52.
go back to reference Wirtz RA, Zavala F, Charoenvit Y, Campbell GH, Burkot TR, Schneider I, et al. Comparative testing of monoclonal antibodies against Plasmodium falciparum sporozoites for ELISA development. Bull World Health Organ. 1987;65:39–45.PubMedPubMedCentral Wirtz RA, Zavala F, Charoenvit Y, Campbell GH, Burkot TR, Schneider I, et al. Comparative testing of monoclonal antibodies against Plasmodium falciparum sporozoites for ELISA development. Bull World Health Organ. 1987;65:39–45.PubMedPubMedCentral
53.
go back to reference Durnez L, Van Bortel W, Denis L, Roelants P, Veracx A, Trung HD, et al. 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.PubMedPubMedCentralCrossRef Durnez L, Van Bortel W, Denis L, Roelants P, Veracx A, Trung HD, et al. 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.PubMedPubMedCentralCrossRef
54.
go back to reference Detinova TS. Age-grouping methods in diptere of medical importance. Geneva: World Health Organization; 1962. Detinova TS. Age-grouping methods in diptere of medical importance. Geneva: World Health Organization; 1962.
55.
go back to reference R Core Team. R: a language and environment for statistical computing. Vienna: R Core Team; 2019. R Core Team. R: a language and environment for statistical computing. Vienna: R Core Team; 2019.
56.
go back to reference Bates D, Mächler M, Bolker BM, Walker SC. Fitting linear mixed-effects models using lme4. J Stat Softw. 2015;67:1–48.CrossRef Bates D, Mächler M, Bolker BM, Walker SC. Fitting linear mixed-effects models using lme4. J Stat Softw. 2015;67:1–48.CrossRef
57.
go back to reference Bolker B. Ecological models and data in R. 2007. Bolker B. Ecological models and data in R. 2007.
58.
go back to reference Ho J, Tumkaya T, Aryal S, Choi H, Claridge-Chang A. Moving beyond P values: everyday data analysis with estimation plots. Nat Methods. 2018;16:565–6.CrossRef Ho J, Tumkaya T, Aryal S, Choi H, Claridge-Chang A. Moving beyond P values: everyday data analysis with estimation plots. Nat Methods. 2018;16:565–6.CrossRef
59.
go back to reference The malERA Refresh Consultative Panel on Tools for Malaria Elimination. malERA: an updated research agenda for diagnostics, drugs, vaccines, and vector control in malaria elimination and eradication. PLoS Med. 2017;14:e1002455.PubMedCentralCrossRef The malERA Refresh Consultative Panel on Tools for Malaria Elimination. malERA: an updated research agenda for diagnostics, drugs, vaccines, and vector control in malaria elimination and eradication. PLoS Med. 2017;14:e1002455.PubMedCentralCrossRef
60.
go back to reference The malERA Consultative Group on Vector Control. A research agenda for malaria eradication: vector control. PLoS Med. 2011;8:e1000401.PubMedCentralCrossRef The malERA Consultative Group on Vector Control. A research agenda for malaria eradication: vector control. PLoS Med. 2011;8:e1000401.PubMedCentralCrossRef
61.
go back to reference Rabinovich RN, Drakeley C, Djimde AA, Hall BF, Hay SI, Hemingway J, et al. malERA: an updated research agenda for malaria elimination and eradication. PLoS Med. 2017;14:e1002456.PubMedPubMedCentralCrossRef Rabinovich RN, Drakeley C, Djimde AA, Hall BF, Hay SI, Hemingway J, et al. malERA: an updated research agenda for malaria elimination and eradication. PLoS Med. 2017;14:e1002456.PubMedPubMedCentralCrossRef
62.
go back to reference Sharp BL, Streat E, Morris N, Kunene S. Seven years of regional malaria control collaboration—Mozambique, South Africa, and Swaziland. Am J Trop Med Hyg. 2007;76:42–7.PubMedCrossRef Sharp BL, Streat E, Morris N, Kunene S. Seven years of regional malaria control collaboration—Mozambique, South Africa, and Swaziland. Am J Trop Med Hyg. 2007;76:42–7.PubMedCrossRef
63.
go back to reference Mabaso MLH, Sharp B, Lengeler C. Historical review of malarial control in southern African with emphasis on the use of indoor residual house-spraying. Trop Med Int Health. 2004;9:846–56.PubMedCrossRef Mabaso MLH, Sharp B, Lengeler C. Historical review of malarial control in southern African with emphasis on the use of indoor residual house-spraying. Trop Med Int Health. 2004;9:846–56.PubMedCrossRef
64.
go back to reference Kisinza WN, Nkya TE, Kabula B, Overgaard HJ, Massue DJ, Mageni Z, et al. Multiple insecticide resistance in Anopheles gambiae from Tanzania: a major concern for malaria vector control. Malar J. 2017;16:439.PubMedPubMedCentralCrossRef Kisinza WN, Nkya TE, Kabula B, Overgaard HJ, Massue DJ, Mageni Z, et al. Multiple insecticide resistance in Anopheles gambiae from Tanzania: a major concern for malaria vector control. Malar J. 2017;16:439.PubMedPubMedCentralCrossRef
Metadata
Title
Preferred resting surfaces of dominant malaria vectors inside different house types in rural south-eastern Tanzania
Authors
Betwel J. Msugupakulya
Emmanuel W. Kaindoa
Halfan S. Ngowo
Japhet M. Kihonda
Najat F. Kahamba
Dickson S. Msaky
Damaris Matoke-Muhia
Patrick K. Tungu
Fredros O. Okumu
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/s12936-020-3108-0

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