Skip to main content
Top
Published in: Malaria Journal 1/2016

Open Access 01-12-2016 | Research

An improved mosquito electrocuting trap that safely reproduces epidemiologically relevant metrics of mosquito human-feeding behaviours as determined by human landing catch

Authors: Nicodem J. Govella, Deodatus F. Maliti, Amos T. Mlwale, John P. Masallu, Nosrat Mirzai, Paul C. D. Johnson, Heather M. Ferguson, Gerry F. Killeen

Published in: Malaria Journal | Issue 1/2016

Login to get access

Abstract

Background

Reliable quantification of mosquito host—seeking behaviours is required to determine the efficacy of vector control methods. For malaria, the gold standard approach remains the risky human landing catch (HLC). Here compare the performance of an improved prototype of the mosquito electrocuting grid trap (MET) as a safer alternative with HLC for measuring malaria vector behaviour in Dar es Salaam, Tanzania.

Methods

Mosquito trapping was conducted at three sites within Dar es Salaam representing a range of urbanicity over a 7-month period (December 2012–July 2013, 168 sampling nights). At each site, sampling was conducted in a block of four houses, with two houses being allocated to HLC and the other to MET on each night of study. Sampling was conducted both indoors and outdoors (from 19:00 to 06:00 each night) at all houses, with trapping method (HLC and MET) being exchanged between pairs of houses at each site using a crossover design.

Results

The MET caught significantly more Anopheles gambiae sensu lato than the HLC, both indoors (RR [95 % confidence interval (CI)]) = 1.47 [1.23–1.76], P < 0.0001 and outdoors = 1.38 [1.14–1.67], P < 0.0001). The sensitivity of MET compared with HLC did not detectably change over the course of night for either An. gambiae s.l. (OR [CI]) = 1.01 [0.94–1.02], P = 0.27) or Culex spp. (OR [CI]) = 0.99 [0.99–1.0], P = 0.17) indoors and declined only slightly outdoors: An. gambiae s.l. (OR [CI]) = 0.92 [0.86–0.99], P = 0.04), and Culex spp. (OR [CI]) = 0.99 [0.98–0.99], P = 0.03). MET-based estimates of the proportions of mosquitoes caught indoors (P i ) or during sleeping hours (P fl ), as well as the proportion of human exposure to bites that would otherwise occurs indoors (π i ), were statistically indistinguishable from those based on HLC for An. gambiae s.l. (P = 0.43, 0.07 and 0.48, respectively) and Culex spp. (P = 0.76, 0.24 and 0.55, respectively).

Conclusions

This improved MET prototype is highly sensitive tool that accurately quantifies epidemiologically-relevant metrics of mosquito biting densities, behaviours and human exposure distribution.
Appendix
Available only for authorised users
Literature
1.
go back to reference Briet OJT, Chitnis N. Effects of changing mosquito host searching behaviours on the cost effectiveness of a mass distribution of long lasting, insecticidal nets: a modelling study. Malar J. 2013;12:215.PubMedPubMedCentralCrossRef Briet OJT, Chitnis N. Effects of changing mosquito host searching behaviours on the cost effectiveness of a mass distribution of long lasting, insecticidal nets: a modelling study. Malar J. 2013;12:215.PubMedPubMedCentralCrossRef
2.
go back to reference Killeen GF, Seyoum A, Gimnig JE, Stevenson JC, Drakeley CJ, Chitnis N. Made-to measure malaria vector control strategies: rational design based on insecticide properties and coverage of blood resources for mosquitoes. Malar J. 2014;13:146.PubMedPubMedCentralCrossRef Killeen GF, Seyoum A, Gimnig JE, Stevenson JC, Drakeley CJ, Chitnis N. Made-to measure malaria vector control strategies: rational design based on insecticide properties and coverage of blood resources for mosquitoes. Malar J. 2014;13:146.PubMedPubMedCentralCrossRef
3.
go back to reference Ferguson HM, Dornhaus A, Beeche A, Borgemeister C, Gottlieb M, Mulla MS, et al. Ecology: a prerequisite for malaria elimination and eradication. PLoS Med. 2010;7:e1000303.PubMedPubMedCentralCrossRef Ferguson HM, Dornhaus A, Beeche A, Borgemeister C, Gottlieb M, Mulla MS, et al. Ecology: a prerequisite for malaria elimination and eradication. PLoS Med. 2010;7:e1000303.PubMedPubMedCentralCrossRef
4.
go back to reference Sougoufara S, Diedhiou SM, Doucoure S, Diagne N, Sembene PM, Harry M, et al. Biting by Anopheles funestus in broad daytime after use of long-lasting insecticidal nets: a new challenge to malaria control. Malar J. 2014;13:125.PubMedPubMedCentralCrossRef Sougoufara S, Diedhiou SM, Doucoure S, Diagne N, Sembene PM, Harry M, et al. Biting by Anopheles funestus in broad daytime after use of long-lasting insecticidal nets: a new challenge to malaria control. Malar J. 2014;13:125.PubMedPubMedCentralCrossRef
5.
go back to reference Geissbühler Y, Chaki P, Emidi B, Govella NJ, Shirima R, Mayagaya V, et al. Interdependence of domestic malaria prevention measures and mosquito-human interactions in urban Dar es Salaam, Tanzania. Malar J. 2007;6:126.PubMedPubMedCentralCrossRef Geissbühler Y, Chaki P, Emidi B, Govella NJ, Shirima R, Mayagaya V, et al. Interdependence of domestic malaria prevention measures and mosquito-human interactions in urban Dar es Salaam, Tanzania. Malar J. 2007;6:126.PubMedPubMedCentralCrossRef
6.
go back to reference Pates H, Curtis C. Mosquito behavior and vector control. Ann Rev Entomol. 2005;50:53–70.CrossRef Pates H, Curtis C. Mosquito behavior and vector control. Ann Rev Entomol. 2005;50:53–70.CrossRef
7.
go back to reference Taylor B. Changes in feeding behaviour on malaria vector, Anopheles farauti Lav., following use of DDT a residual spray in houses in the British Solomon Island Protectorate. Trans R Entomol Soc. 1975;127:277–92.CrossRef Taylor B. Changes in feeding behaviour on malaria vector, Anopheles farauti Lav., following use of DDT a residual spray in houses in the British Solomon Island Protectorate. Trans R Entomol Soc. 1975;127:277–92.CrossRef
8.
go back to reference Bugoro H, Cooper RD, Butafa C, Iro’ofa C, Mackenzie DO, Chen C, et al. Bionomics of the malaria vector Anopheles farauti in Temotu Province, Solomon Islands: issues for malaria elimination. Malar J. 2011;10:133.PubMedPubMedCentralCrossRef Bugoro H, Cooper RD, Butafa C, Iro’ofa C, Mackenzie DO, Chen C, et al. Bionomics of the malaria vector Anopheles farauti in Temotu Province, Solomon Islands: issues for malaria elimination. Malar J. 2011;10:133.PubMedPubMedCentralCrossRef
9.
go back to reference Moiroux N, Damien GB, Egrot M, Djenontin A, Chandre F, Corbel V, et al. Human exposure to early morning Anopheles funestus biting behavior and personal protection provided by long-lasting insecticidal nets. PLoS One. 2014;9:e104967.PubMedPubMedCentralCrossRef Moiroux N, Damien GB, Egrot M, Djenontin A, Chandre F, Corbel V, et al. Human exposure to early morning Anopheles funestus biting behavior and personal protection provided by long-lasting insecticidal nets. PLoS One. 2014;9:e104967.PubMedPubMedCentralCrossRef
10.
go back to reference Trung HD, Bortel WV, Sochantha T, Keokenchanh K, Briet OJT. Behavioural heterogeneity of Anopheles species in ecologically different localities in southeast Asia: a challenge for vector control. Trop Med Int Health. 2005;10:251–62.PubMedCrossRef Trung HD, Bortel WV, Sochantha T, Keokenchanh K, Briet OJT. Behavioural heterogeneity of Anopheles species in ecologically different localities in southeast Asia: a challenge for vector control. Trop Med Int Health. 2005;10:251–62.PubMedCrossRef
11.
go back to reference Rubio-Palis Y, Curtis CF. Biting and resting behaviour of Anophelines in western Venezuela and implications for control of malaria transmission. Med Vet Entomol. 1992;6:325–34.PubMedCrossRef Rubio-Palis Y, Curtis CF. Biting and resting behaviour of Anophelines in western Venezuela and implications for control of malaria transmission. Med Vet Entomol. 1992;6:325–34.PubMedCrossRef
12.
go back to reference Ahumada ML, Pareja PX, Buitrago LS, Quinones ML. Biting behaviours of Anopheles darling Root, 1926 (Diptera: Culicidae) and its association with malaria transmission in Villavicencio (Meta, Colombia). Biomedica. 2013;33:241–50.PubMed Ahumada ML, Pareja PX, Buitrago LS, Quinones ML. Biting behaviours of Anopheles darling Root, 1926 (Diptera: Culicidae) and its association with malaria transmission in Villavicencio (Meta, Colombia). Biomedica. 2013;33:241–50.PubMed
13.
go back to reference Bockarie MJ, Pedersen EM, White GB, Michael E. Role of vector control in the global program to eradicate lymphatic filariasis. Ann Rev Entomol. 2009;54:469–87.CrossRef Bockarie MJ, Pedersen EM, White GB, Michael E. Role of vector control in the global program to eradicate lymphatic filariasis. Ann Rev Entomol. 2009;54:469–87.CrossRef
14.
go back to reference Simonsen PE, Pedersen EM, Rwegoshora RT, Malecela MN, Derua YA, Magesa SM. Lymphatic filariasis control in Tanzania: effect of repeated mass drug administration with ivermectin and albendazole on infection and transmission. PLoS Negl Trop Dis. 2010;4:e696.PubMedPubMedCentralCrossRef Simonsen PE, Pedersen EM, Rwegoshora RT, Malecela MN, Derua YA, Magesa SM. Lymphatic filariasis control in Tanzania: effect of repeated mass drug administration with ivermectin and albendazole on infection and transmission. PLoS Negl Trop Dis. 2010;4:e696.PubMedPubMedCentralCrossRef
15.
go back to reference Uttah EC, Wokem GN, Okonofua C. The abundance and biting patterns of Culex quinquefasciatus Say (Culicidae) in the Coast region of Nigeria. ISRN Zool. 2013;2013:1–7.CrossRef Uttah EC, Wokem GN, Okonofua C. The abundance and biting patterns of Culex quinquefasciatus Say (Culicidae) in the Coast region of Nigeria. ISRN Zool. 2013;2013:1–7.CrossRef
16.
go back to reference Govella NJ, Chaki PP, Killeen GF. Entomological surveillance of behavioural resilience and resistance in residual malaria vector populations. Malar J. 2013;12:124.PubMedPubMedCentralCrossRef Govella NJ, Chaki PP, Killeen GF. Entomological surveillance of behavioural resilience and resistance in residual malaria vector populations. Malar J. 2013;12:124.PubMedPubMedCentralCrossRef
17.
go back to reference Huho B, Briet OJT, Seyoum A, Sikala C, Bayoh N, Gimnig JE, et al. Consistently high estimates for proportion of human exposure to malaria vector populations occurring indoors in rural Africa. Int J Epidemiol. 2013;42:235–47.PubMedPubMedCentralCrossRef Huho B, Briet OJT, Seyoum A, Sikala C, Bayoh N, Gimnig JE, et al. Consistently high estimates for proportion of human exposure to malaria vector populations occurring indoors in rural Africa. Int J Epidemiol. 2013;42:235–47.PubMedPubMedCentralCrossRef
19.
go back to reference Lindblade KA. Does a mosquito bite when no one is around to hear it. Int J Epidemiol. 2013;42:247–9.PubMedCrossRef Lindblade KA. Does a mosquito bite when no one is around to hear it. Int J Epidemiol. 2013;42:247–9.PubMedCrossRef
20.
go back to reference Killeen GF, Kihonda J, Lyimo E, Oketch FR, Kotas ME, Mathenge E, et al. Quantifying behavioural interactions between humans and mosquitoes: evaluating the protective efficacy of insecticidal nets against malaria transmission in rural Tanzania. BMC Infect Dis. 2006;6:161.PubMedPubMedCentralCrossRef Killeen GF, Kihonda J, Lyimo E, Oketch FR, Kotas ME, Mathenge E, et al. Quantifying behavioural interactions between humans and mosquitoes: evaluating the protective efficacy of insecticidal nets against malaria transmission in rural Tanzania. BMC Infect Dis. 2006;6:161.PubMedPubMedCentralCrossRef
21.
go back to reference Seyoum A, Sikala C, Chanda J, Chinula D, Ntamatungiro AJ, Hawela M, et al. Human exposure to Anopheline mosquitoes occurs primarily indoors, even for users of insecticide-treated nets in Luangwa valley, South-east Zambia. Parasit Vectors. 2012;5:101.PubMedPubMedCentralCrossRef Seyoum A, Sikala C, Chanda J, Chinula D, Ntamatungiro AJ, Hawela M, et al. Human exposure to Anopheline mosquitoes occurs primarily indoors, even for users of insecticide-treated nets in Luangwa valley, South-east Zambia. Parasit Vectors. 2012;5:101.PubMedPubMedCentralCrossRef
22.
go back to reference Wong ML, Chua TH, Leong CS, Khaw LT, Fornace K, Wan-Sulaiman WY, et al. Seasonal and spatial dynamics of the primary vector of Plasmodium Knowlesi within major transmission focus in Sabah, Malaysia. PLoS Negl Trop Dis. 2015;9:e0004135.PubMedPubMedCentralCrossRef Wong ML, Chua TH, Leong CS, Khaw LT, Fornace K, Wan-Sulaiman WY, et al. Seasonal and spatial dynamics of the primary vector of Plasmodium Knowlesi within major transmission focus in Sabah, Malaysia. PLoS Negl Trop Dis. 2015;9:e0004135.PubMedPubMedCentralCrossRef
24.
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.PubMed Pluess B, Tanser FC, Lengeler C, Sharp BL. Indoor residual spraying for preventing malaria. Cochrane Database Syst Rev. 2010;4:CD006657.PubMed
25.
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
26.
go back to reference UNICEF, WHO. Achieving the malaria MDG target: reversing the incidence of malaria 2000–2015. Geneva: World Health Organization and the United Nations Children’s Fund; 2015. p. 1–32. UNICEF, WHO. Achieving the malaria MDG target: reversing the incidence of malaria 2000–2015. Geneva: World Health Organization and the United Nations Children’s Fund; 2015. p. 1–32.
27.
go back to reference Simonsen PE, Malecela MN, Michael E, Mackenzie CD. Lymphatic filariasis research and control in Eastern and Southern Africa. Frederiksberg: DBL-Centre for Health Research and Development; 2008. Simonsen PE, Malecela MN, Michael E, Mackenzie CD. Lymphatic filariasis research and control in Eastern and Southern Africa. Frederiksberg: DBL-Centre for Health Research and Development; 2008.
28.
go back to reference WHO. Global programme to eliminate lymphatic filariasis. Lymphatic filariasis: practical entomology. Geneva: World Health Organization; 2013. WHO. Global programme to eliminate lymphatic filariasis. Lymphatic filariasis: practical entomology. Geneva: World Health Organization; 2013.
29.
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.PubMedPubMedCentralCrossRef 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.PubMedPubMedCentralCrossRef
30.
go back to reference Derua YA, Alifrangis M, Hosea KM, Meyrowitsch DW, Magessa SM, Pedersen EM, et al. Change in composition of Anopheles gambiae complex and its possible implications for the transmission of malaria and lymphatic filariasis in north-eastern Tanzania. Malar J. 2012;11:188.PubMedPubMedCentralCrossRef Derua YA, Alifrangis M, Hosea KM, Meyrowitsch DW, Magessa SM, Pedersen EM, et al. Change in composition of Anopheles gambiae complex and its possible implications for the transmission of malaria and lymphatic filariasis in north-eastern Tanzania. Malar J. 2012;11:188.PubMedPubMedCentralCrossRef
31.
go back to reference Bayoh MN, Mathias DK, Odiere MR, Mutuku FM, Kamau L, Gimnig JE, et al. Anopheles gambiae: historical population decline associated with regional distribution of insecticide-treated bed nets in Western Nyanza Province, Kenya. Malar J. 2010;9:62.PubMedPubMedCentralCrossRef Bayoh MN, Mathias DK, Odiere MR, Mutuku FM, Kamau L, Gimnig JE, et al. Anopheles gambiae: historical population decline associated with regional distribution of insecticide-treated bed nets in Western Nyanza Province, Kenya. Malar J. 2010;9:62.PubMedPubMedCentralCrossRef
32.
go back to reference Mwangangi JM, Mbogo CM, Orindi BO, Muturi EJ, Midega JT, Nzovu J, et al. Shifts in malaria vector species composition and transmission dynamics along the Kenyan coast over the past 20 years. Malar J. 2013;12:13.PubMedPubMedCentralCrossRef Mwangangi JM, Mbogo CM, Orindi BO, Muturi EJ, Midega JT, Nzovu J, et al. Shifts in malaria vector species composition and transmission dynamics along the Kenyan coast over the past 20 years. Malar J. 2013;12:13.PubMedPubMedCentralCrossRef
33.
go back to reference Gatton ML, Chitnis N, Churcher T, Donnelly MJ, Ghani AC, Godfray HC, et al. The importance of mosquito behavioural adaptations to malaria control in Africa. Evolution. 2013;67:1218–30.PubMedPubMedCentralCrossRef Gatton ML, Chitnis N, Churcher T, Donnelly MJ, Ghani AC, Godfray HC, et al. The importance of mosquito behavioural adaptations to malaria control in Africa. Evolution. 2013;67:1218–30.PubMedPubMedCentralCrossRef
34.
go back to reference Russell TL, Beebe NW, Cooper RD, Lobo NF, Burkot TR. Successful malaria elimination strategies require interventions that target changing vector behaviours. Malar J. 2013;12:56.PubMedPubMedCentralCrossRef Russell TL, Beebe NW, Cooper RD, Lobo NF, Burkot TR. Successful malaria elimination strategies require interventions that target changing vector behaviours. Malar J. 2013;12:56.PubMedPubMedCentralCrossRef
35.
36.
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
37.
go back to reference Briet OJT, Huho B, Gimnig JE, Bayoh N, Seyoum A, Sikaala C, et al. Applications and limitations of Centers for Disease Control and Prevention miniature light traps for measuring biting densities of African malaria vector populations: a pooled analysis of 13 comparisons with human landing catches. Malar J. 2015;14:247.PubMedPubMedCentralCrossRef Briet OJT, Huho B, Gimnig JE, Bayoh N, Seyoum A, Sikaala C, et al. Applications and limitations of Centers for Disease Control and Prevention miniature light traps for measuring biting densities of African malaria vector populations: a pooled analysis of 13 comparisons with human landing catches. Malar J. 2015;14:247.PubMedPubMedCentralCrossRef
38.
go back to reference Mboera LEG. Sampling techniques for adult Afrotropical malaria vectors and their reliability in the estimation of entomological inoculation rates. Tanzania Health Res Bull. 2005;7:117–24. Mboera LEG. Sampling techniques for adult Afrotropical malaria vectors and their reliability in the estimation of entomological inoculation rates. Tanzania Health Res Bull. 2005;7:117–24.
39.
go back to reference Govella NJ, Chaki PP, Geissbühler Y, Kannady K, Okumu FO, Charlwood JD, et al. A new tent trap for sampling exophagic and endophagic members of the Anopheles gambiae complex. Malar J. 2009;8:157.PubMedPubMedCentralCrossRef Govella NJ, Chaki PP, Geissbühler Y, Kannady K, Okumu FO, Charlwood JD, et al. A new tent trap for sampling exophagic and endophagic members of the Anopheles gambiae complex. Malar J. 2009;8:157.PubMedPubMedCentralCrossRef
40.
go back to reference Govella NJ, Chaki PP, Mpangile J, Killeen GF. Monitoring mosquitoes in urban Dar es Salaam: evaluation of resting boxes, window exit traps, CDC light traps, Ifakara tent traps and human landing catches. Parasit Vectors. 2011;4:40.PubMedPubMedCentralCrossRef Govella NJ, Chaki PP, Mpangile J, Killeen GF. Monitoring mosquitoes in urban Dar es Salaam: evaluation of resting boxes, window exit traps, CDC light traps, Ifakara tent traps and human landing catches. Parasit Vectors. 2011;4:40.PubMedPubMedCentralCrossRef
41.
42.
go back to reference Chaki PP, Mlacha Y, Msellem D, Muhili A, Malishee AD, Mtema ZJ, et al. An affordable, quality-assured community-based system for high-resolution entomological surveillance of vector mosquitoes that reflects human malaria infection risk pattern. Malar J. 2012;11:172.PubMedPubMedCentralCrossRef Chaki PP, Mlacha Y, Msellem D, Muhili A, Malishee AD, Mtema ZJ, et al. An affordable, quality-assured community-based system for high-resolution entomological surveillance of vector mosquitoes that reflects human malaria infection risk pattern. Malar J. 2012;11:172.PubMedPubMedCentralCrossRef
43.
go back to reference Mathenge EM, Misiani GO, Oulo DO, Irungu LW, Ndegwa P, Smith TA, et al. Comparative performance of the Mbita trap, CDC light trap and the human landing catch in the sampling of Anopheles arabiensis, An. funestus and culicine species in a rice irrigation scheme in western Kenya. Malar J. 2005;4:7.PubMedPubMedCentralCrossRef Mathenge EM, Misiani GO, Oulo DO, Irungu LW, Ndegwa P, Smith TA, et al. Comparative performance of the Mbita trap, CDC light trap and the human landing catch in the sampling of Anopheles arabiensis, An. funestus and culicine species in a rice irrigation scheme in western Kenya. Malar J. 2005;4:7.PubMedPubMedCentralCrossRef
44.
go back to reference Mathenge EM, Omweri GO, Irungu LW, Ndegwa PN, Walczak E, Smith TA, et al. Comparative field evaluation of the Mbita trap, the Centers for Disease Control light trap, and the human landing catch for sampling of malaria vectors in western Kenya. Am J Trop Med Hyg. 2004;70:33–7.PubMed Mathenge EM, Omweri GO, Irungu LW, Ndegwa PN, Walczak E, Smith TA, et al. Comparative field evaluation of the Mbita trap, the Centers for Disease Control light trap, and the human landing catch for sampling of malaria vectors in western Kenya. Am J Trop Med Hyg. 2004;70:33–7.PubMed
45.
go back to reference Bradley J, Lines J, Fuseini G, Schwabe C, Monti F, Slotman M, et al. Outdoor biting by Anopheles mosquitoes on Bioko Island does not currently impact on malaria control. Malar J. 2015;14:170.PubMedPubMedCentralCrossRef Bradley J, Lines J, Fuseini G, Schwabe C, Monti F, Slotman M, et al. Outdoor biting by Anopheles mosquitoes on Bioko Island does not currently impact on malaria control. Malar J. 2015;14:170.PubMedPubMedCentralCrossRef
46.
go back to reference Reddy MR, Overgaard HJ, Abaga S, Reddy VP, Caccone A, Kiszewski AE, et al. Outdoor host seeking behaviour of Anopheles gambiae mosquitoes following initiation of malaria vector control on Bioko Island, Equatorial Guinea. Malar J. 2011;10:184.PubMedPubMedCentralCrossRef Reddy MR, Overgaard HJ, Abaga S, Reddy VP, Caccone A, Kiszewski AE, et al. Outdoor host seeking behaviour of Anopheles gambiae mosquitoes following initiation of malaria vector control on Bioko Island, Equatorial Guinea. Malar J. 2011;10:184.PubMedPubMedCentralCrossRef
47.
go back to reference Lima JBP, Rosa-Freitas MG, Rodovalho CM, Santos F, Lourenco-de-Oliveira R. Is there an efficient trap or collection method for sampling Anopheles darlingi and other malaria vectors that can describe the essential parameters affecting transmission dynamics as effectively as human landing catches? A review. Mem Inst Oswaldo Cruz. 2014;109:685–705.PubMedPubMedCentralCrossRef Lima JBP, Rosa-Freitas MG, Rodovalho CM, Santos F, Lourenco-de-Oliveira R. Is there an efficient trap or collection method for sampling Anopheles darlingi and other malaria vectors that can describe the essential parameters affecting transmission dynamics as effectively as human landing catches? A review. Mem Inst Oswaldo Cruz. 2014;109:685–705.PubMedPubMedCentralCrossRef
48.
go back to reference Achee NL, Youngblood L, Bangs MJ, Lavery JV, James S. Considerations for the use of human participants in vector biology research. Vector Borne Zoonotic Dis. 2015;15:89–102.PubMedPubMedCentralCrossRef Achee NL, Youngblood L, Bangs MJ, Lavery JV, James S. Considerations for the use of human participants in vector biology research. Vector Borne Zoonotic Dis. 2015;15:89–102.PubMedPubMedCentralCrossRef
49.
go back to reference Sikaala C, Killeen GF, Chanda J, Chinula D, Miller JM, Russell TL, et al. Evaluation of alternative mosquito sampling methods for malaria vectors in lowland south east Zambia. Parasit Vectors. 2013;6:91.PubMedPubMedCentralCrossRef Sikaala C, Killeen GF, Chanda J, Chinula D, Miller JM, Russell TL, et al. Evaluation of alternative mosquito sampling methods for malaria vectors in lowland south east Zambia. Parasit Vectors. 2013;6:91.PubMedPubMedCentralCrossRef
50.
go back to reference Sadanandane C, Jambulingam P, Subramanian S. Role of modified CDC miniature light-traps as an alternative method for sampling adult Anophelines (Diptera: Culicidae) in the National Mosquito Surveillance Programme in India. Bull Entomol Res. 2013;94:55–64. Sadanandane C, Jambulingam P, Subramanian S. Role of modified CDC miniature light-traps as an alternative method for sampling adult Anophelines (Diptera: Culicidae) in the National Mosquito Surveillance Programme in India. Bull Entomol Res. 2013;94:55–64.
51.
go back to reference Costantini C, Sagnon NF, Sanogo E, Merzagora L, Colluzi M. Relationship to human biting collections and influence of light and bednets in CDC light-trap catches of West African malaria vectors. Bull Entomol Res. 1998;88:503–11.CrossRef Costantini C, Sagnon NF, Sanogo E, Merzagora L, Colluzi M. Relationship to human biting collections and influence of light and bednets in CDC light-trap catches of West African malaria vectors. Bull Entomol Res. 1998;88:503–11.CrossRef
52.
go back to reference Faye O, Diallo S, Gaye O, Ndir O. Efficacité comparée de l’utilisation des pièges lumineux du type CDC et des sujets humains pour l’échantillonnage des populations anophéliennes. Résultats obtenus dans la zone de Bignona. Bull Soc Pathol Exot. 1992;85:185–9.PubMed Faye O, Diallo S, Gaye O, Ndir O. Efficacité comparée de l’utilisation des pièges lumineux du type CDC et des sujets humains pour l’échantillonnage des populations anophéliennes. Résultats obtenus dans la zone de Bignona. Bull Soc Pathol Exot. 1992;85:185–9.PubMed
53.
go back to reference Overgaard HJ, Saebo S, Reddy MR, Reddy VP, Abaga S, Matias A, et al. Light traps fail to estimate reliable malaria mosquito biting rates on Bioko Island, Equatorial Guinea. Malar J. 2012;11:56.PubMedPubMedCentralCrossRef Overgaard HJ, Saebo S, Reddy MR, Reddy VP, Abaga S, Matias A, et al. Light traps fail to estimate reliable malaria mosquito biting rates on Bioko Island, Equatorial Guinea. Malar J. 2012;11:56.PubMedPubMedCentralCrossRef
54.
go back to reference Service MW. Mosquito ecology-field sampling methods. New York: John Wiley and Sons; 1977. Service MW. Mosquito ecology-field sampling methods. New York: John Wiley and Sons; 1977.
55.
go back to reference Service MW. A critical review of procedures for sampling populations of adult mosquitoes. Bull Entomol Res. 1977;67:343–82.CrossRef Service MW. A critical review of procedures for sampling populations of adult mosquitoes. Bull Entomol Res. 1977;67:343–82.CrossRef
56.
go back to reference WHO. Malaria entomology and vector control. Learner’s guide. 3rd ed. Geneva: World Health Organization; 2002. WHO. Malaria entomology and vector control. Learner’s guide. 3rd ed. Geneva: World Health Organization; 2002.
57.
go back to reference Ndebele P, Musesengwa R. View Point: ethical dilemmas in malaria vector research in Africa: Making the difficult choice between mosquito, science and humans. Malawi Med J. 2012;24:65–8.PubMedPubMedCentral Ndebele P, Musesengwa R. View Point: ethical dilemmas in malaria vector research in Africa: Making the difficult choice between mosquito, science and humans. Malawi Med J. 2012;24:65–8.PubMedPubMedCentral
58.
go back to reference Gimnig JE, Walker ED, Otieno P, Kosgei J, Olang G, Omboki M, et al. Incidence of malaria among mosquito collectors conducting human landing catches in western Kenya. Am J Trop Med Hyg. 2013;88:301–8.PubMedPubMedCentralCrossRef Gimnig JE, Walker ED, Otieno P, Kosgei J, Olang G, Omboki M, et al. Incidence of malaria among mosquito collectors conducting human landing catches in western Kenya. Am J Trop Med Hyg. 2013;88:301–8.PubMedPubMedCentralCrossRef
59.
go back to reference Moi ML, Takasaki T, Kotaki A, Tajima S, Lim C, Sakamoto M, et al. Importation of dengue virus type 3 to Japan from Tanzania and Cote d’Ivoire. Emerg Infect Dis. 2010;16:1770–2.PubMedPubMedCentralCrossRef Moi ML, Takasaki T, Kotaki A, Tajima S, Lim C, Sakamoto M, et al. Importation of dengue virus type 3 to Japan from Tanzania and Cote d’Ivoire. Emerg Infect Dis. 2010;16:1770–2.PubMedPubMedCentralCrossRef
60.
go back to reference Chretien J, Anyamba A, Bedno S, Breiman SF, Sang R, Sergon K, et al. Drought associated Ckikungunya emergency along coastal East Africa. Am J Trop Med Hyg. 2007;76:405–7.PubMed Chretien J, Anyamba A, Bedno S, Breiman SF, Sang R, Sergon K, et al. Drought associated Ckikungunya emergency along coastal East Africa. Am J Trop Med Hyg. 2007;76:405–7.PubMed
61.
go back to reference Faye O, Freire CM, Lamarino A, Faye O, de Oliveira JVC, Diallo M. Molecular evolution of Zika virus during its emergence in the 20th Century. PLoS Negl Trop Dis. 2014;8:e2634.CrossRef Faye O, Freire CM, Lamarino A, Faye O, de Oliveira JVC, Diallo M. Molecular evolution of Zika virus during its emergence in the 20th Century. PLoS Negl Trop Dis. 2014;8:e2634.CrossRef
62.
go back to reference Musso D, Cao-Lormeau VM, Gubler DJ. Zika virus: following the path of dengue and chikungunya? Lancet. 2015;386:243–4.PubMedCrossRef Musso D, Cao-Lormeau VM, Gubler DJ. Zika virus: following the path of dengue and chikungunya? Lancet. 2015;386:243–4.PubMedCrossRef
63.
go back to reference Govella NJ, Okumu FO, Killeen GF. Insecticide-treated nets can reduce malaria transmission by mosquitoes which feed outdoors. Am J Trop Med Hyg. 2010;82:415–9.PubMedPubMedCentralCrossRef Govella NJ, Okumu FO, Killeen GF. Insecticide-treated nets can reduce malaria transmission by mosquitoes which feed outdoors. Am J Trop Med Hyg. 2010;82:415–9.PubMedPubMedCentralCrossRef
64.
go back to reference Cook MK, Kahindi SC, Oriango RM, Owaga C, Ayoma E, Mabuka D, et al. A bite before bed’: exposure to malaria vectors outside the times of net use in the highlands of western Kenya. Malar J. 2015;14:259.CrossRef Cook MK, Kahindi SC, Oriango RM, Owaga C, Ayoma E, Mabuka D, et al. A bite before bed’: exposure to malaria vectors outside the times of net use in the highlands of western Kenya. Malar J. 2015;14:259.CrossRef
65.
go back to reference Msellemu D, Namango HI, Mwakalinga VM, Ntamatungiro AJ, Mlacha Y, Mtema ZJ, et al. The epidemiology of residual Plasmodium falciparum malaria transmission and infection burden in an African city with high coverage of multiple vector control measures. Malar J. 2016;15:288.PubMedPubMedCentralCrossRef Msellemu D, Namango HI, Mwakalinga VM, Ntamatungiro AJ, Mlacha Y, Mtema ZJ, et al. The epidemiology of residual Plasmodium falciparum malaria transmission and infection burden in an African city with high coverage of multiple vector control measures. Malar J. 2016;15:288.PubMedPubMedCentralCrossRef
66.
go back to reference Garrett-Jones C. Epidemiological entomology and its application-to malaria. Geneva: World Health Organization; 1968. Garrett-Jones C. Epidemiological entomology and its application-to malaria. Geneva: World Health Organization; 1968.
67.
go back to reference Majambere S, Masue D, Mlacha Y, Govella NJ, Magesa SM, Killeen GF. Advantages and limitations of commercially available electrocuting grids for studying mosquito behaviour. Parasit Vectors. 2013;6:53.PubMedPubMedCentralCrossRef Majambere S, Masue D, Mlacha Y, Govella NJ, Magesa SM, Killeen GF. Advantages and limitations of commercially available electrocuting grids for studying mosquito behaviour. Parasit Vectors. 2013;6:53.PubMedPubMedCentralCrossRef
68.
go back to reference Maliti DF, Govella NJ, Killeen GF, Mirzai N, Johnson PCD, Kreppel K, et al. Development and evaluation of mosquito-electrocuting traps as alternatives to the human landing catch technique for sampling host-seeking malaria vectors. Malar J. 2015;14:502.PubMedPubMedCentralCrossRef Maliti DF, Govella NJ, Killeen GF, Mirzai N, Johnson PCD, Kreppel K, et al. Development and evaluation of mosquito-electrocuting traps as alternatives to the human landing catch technique for sampling host-seeking malaria vectors. Malar J. 2015;14:502.PubMedPubMedCentralCrossRef
69.
go back to reference NBS. Population and housing census: population distribution by 2013. Nigeria: National Bureau of Statistics; 2012. NBS. Population and housing census: population distribution by 2013. Nigeria: National Bureau of Statistics; 2012.
70.
go back to reference Geissbühler Y, Kannady K, Chaki PP, Emidi B, Govella NJ, Mayagaya V, et al. Microbial larvicide application by a large-scale, community-based program reduces malaria infection prevalence in Urban Dar Es Salaam, Tanzania. PLoS One. 2009;4:e5107.PubMedPubMedCentralCrossRef Geissbühler Y, Kannady K, Chaki PP, Emidi B, Govella NJ, Mayagaya V, et al. Microbial larvicide application by a large-scale, community-based program reduces malaria infection prevalence in Urban Dar Es Salaam, Tanzania. PLoS One. 2009;4:e5107.PubMedPubMedCentralCrossRef
71.
go back to reference NBS. Tanzania HIV/AIDS and Malaria Indicator Survey 2011–2012. Nigeria: National Bureau of Statistics; 2013. p. 1–229. NBS. Tanzania HIV/AIDS and Malaria Indicator Survey 2011–2012. Nigeria: National Bureau of Statistics; 2013. p. 1–229.
72.
go back to reference Ogoma SB, Kannady K, Sikulu M, Chaki PP, Govella NJ, Mukabana WR, et al. Window screening, ceilings and closed eaves as sustainable ways to control malaria in Dar es Salaam, Tanzania. Malar J. 2009;8:221.PubMedPubMedCentralCrossRef Ogoma SB, Kannady K, Sikulu M, Chaki PP, Govella NJ, Mukabana WR, et al. Window screening, ceilings and closed eaves as sustainable ways to control malaria in Dar es Salaam, Tanzania. Malar J. 2009;8:221.PubMedPubMedCentralCrossRef
73.
go back to reference Castro MC, Tsuruta A, Kanamori S, Kannady K, Mkude S. Community-based environmental management for malaria control: evidence from a small-scale intervention in Dar es Salaam, Tanzania. Malar J. 2009;8:57.PubMedPubMedCentralCrossRef Castro MC, Tsuruta A, Kanamori S, Kannady K, Mkude S. Community-based environmental management for malaria control: evidence from a small-scale intervention in Dar es Salaam, Tanzania. Malar J. 2009;8:57.PubMedPubMedCentralCrossRef
74.
go back to reference Castro MC, Kanamori S, Kannady K, Mkude S, Killeen GF, Fillinger U. The importance of drains for the larval development of lymphatic filariasis and malaria vectors in Dar es salaam, United Republic of Tanzania. PLoS Negl Trop Dis. 2010;4:e693.PubMedPubMedCentralCrossRef Castro MC, Kanamori S, Kannady K, Mkude S, Killeen GF, Fillinger U. The importance of drains for the larval development of lymphatic filariasis and malaria vectors in Dar es salaam, United Republic of Tanzania. PLoS Negl Trop Dis. 2010;4:e693.PubMedPubMedCentralCrossRef
75.
go back to reference Gillies MT, DeMeillon B. The Anophelinae of Africa south of the Sahara (Ethiopian zoogeographical region). Johannesburg: South African Institute for Medical Research; 1968. Gillies MT, DeMeillon B. The Anophelinae of Africa south of the Sahara (Ethiopian zoogeographical region). Johannesburg: South African Institute for Medical Research; 1968.
76.
go back to reference Chavasse DC, Lines JD, Ichimori K, Marijani J. Mosquito control in Dar es Salaam. I. Assessment of Culex quinquefasciatus breeding sites prior to intervention. Med Vet Entomol. 1995;9:141–6.PubMedCrossRef Chavasse DC, Lines JD, Ichimori K, Marijani J. Mosquito control in Dar es Salaam. I. Assessment of Culex quinquefasciatus breeding sites prior to intervention. Med Vet Entomol. 1995;9:141–6.PubMedCrossRef
77.
go back to reference Chavasse DC, Lines JD, Ichimori K, Majala AR, Minjas JN, Marijani J. Mosquito control in Dar es Salaam. II. Impact of expanded polystyrene beads and pyriproxyfen treatment of breeding sites on Culex quinquefasciatus densities. Med Vet Entomol. 1995;9:147–54.PubMedCrossRef Chavasse DC, Lines JD, Ichimori K, Majala AR, Minjas JN, Marijani J. Mosquito control in Dar es Salaam. II. Impact of expanded polystyrene beads and pyriproxyfen treatment of breeding sites on Culex quinquefasciatus densities. Med Vet Entomol. 1995;9:147–54.PubMedCrossRef
78.
go back to reference Stephens C, Masamu ET, Kiama MG, Keto AJ, Kinenekejo M, Ichimori K, et al. Knowledge of mosquitos in relation to public and domestic control activities in the cities of Dar es Salaam and Tanga. Bull World Health Organ. 1995;73:97–104.PubMedPubMedCentral Stephens C, Masamu ET, Kiama MG, Keto AJ, Kinenekejo M, Ichimori K, et al. Knowledge of mosquitos in relation to public and domestic control activities in the cities of Dar es Salaam and Tanga. Bull World Health Organ. 1995;73:97–104.PubMedPubMedCentral
79.
go back to reference Malecela MN, Lazarus W, Mwingira U, Mwakitalu E, Makene C, Kabali C, et al. A progress report from Tanzania. J Lymphoedema. 2009;4:10–2. Malecela MN, Lazarus W, Mwingira U, Mwakitalu E, Makene C, Kabali C, et al. A progress report from Tanzania. J Lymphoedema. 2009;4:10–2.
80.
go back to reference Maliti DF. Ecological and genetic determinants of malaria vectors feeding and resting behaviours. Glasgow: University of Glasgow, Institute of Biodiversity, Animal Health and Comparative Medicine, School of Life Sciences, College of Medical, Veterinary and Life Sciences; 2015. Maliti DF. Ecological and genetic determinants of malaria vectors feeding and resting behaviours. Glasgow: University of Glasgow, Institute of Biodiversity, Animal Health and Comparative Medicine, School of Life Sciences, College of Medical, Veterinary and Life Sciences; 2015.
81.
go back to reference WHO. Manual on practical entomology. Part 2. Methods and techniques. Vol 13. Geneva: World Health Organization; 1975. WHO. Manual on practical entomology. Part 2. Methods and techniques. Vol 13. Geneva: World Health Organization; 1975.
82.
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.
83.
go back to reference Scott JA, Brogdon WG, Collins FH. Identification of single specimens of Anopheles gambiae complex by polymerase chain reaction. Am J Trop Med Hyg. 1993;49:520–9.PubMed Scott JA, Brogdon WG, Collins FH. Identification of single specimens of Anopheles gambiae complex by polymerase chain reaction. Am J Trop Med Hyg. 1993;49:520–9.PubMed
84.
go back to reference Wirtz RAF, Zavala Y, Charoenvit GH, Campbell TR, Burkot I, Schmeider KM, et al. Comperative testing of monoclonal antibodies against Plasmodium falciparum sporozoites for ELISA development. Bull World Health Organ. 1987;65:39–45.PubMedPubMedCentral Wirtz RAF, Zavala Y, Charoenvit GH, Campbell TR, Burkot I, Schmeider KM, et al. Comperative testing of monoclonal antibodies against Plasmodium falciparum sporozoites for ELISA development. Bull World Health Organ. 1987;65:39–45.PubMedPubMedCentral
85.
go back to reference Wirtz RA, Duncan JF, Njelesani EK, Schneider I, Brown AE, Oster CN, et al. ELISA method for detecting Plasmodium falciparum circumsporozoite antibody. Bull World Health Org. 1989;67:535–42.PubMedPubMedCentral Wirtz RA, Duncan JF, Njelesani EK, Schneider I, Brown AE, Oster CN, et al. ELISA method for detecting Plasmodium falciparum circumsporozoite antibody. Bull World Health Org. 1989;67:535–42.PubMedPubMedCentral
86.
go back to reference Hii JLK, Smith T, Mai A, Ibam E, Alpers MP. Comparison between anopheline mosquitoes (Diptera: Culicidae) caught using different methods in a malaria endemic area of Papua New Guinea. Bull Entomol Res. 2000;90:211–9.PubMedCrossRef Hii JLK, Smith T, Mai A, Ibam E, Alpers MP. Comparison between anopheline mosquitoes (Diptera: Culicidae) caught using different methods in a malaria endemic area of Papua New Guinea. Bull Entomol Res. 2000;90:211–9.PubMedCrossRef
87.
go back to reference Plummer M. JAGS: a Program for Analysis of Bayesian Graphical Models Using Gibbs Sampling. In: Proceedings of the 3rd international workshop on distributed statistical computing (DSC 2003). Vienna; 2003. Plummer M. JAGS: a Program for Analysis of Bayesian Graphical Models Using Gibbs Sampling. In: Proceedings of the 3rd international workshop on distributed statistical computing (DSC 2003). Vienna; 2003.
89.
go back to reference Matos CA, Thomas DL, Gianola D, Tempelman RJ, Young LD. Genetic analysis of discrete reproductive traits in sheep using linear and nonlinear models: I. Estimation of genetic parameters. J Anim Sci. 1997;75:76–87.PubMedCrossRef Matos CA, Thomas DL, Gianola D, Tempelman RJ, Young LD. Genetic analysis of discrete reproductive traits in sheep using linear and nonlinear models: I. Estimation of genetic parameters. J Anim Sci. 1997;75:76–87.PubMedCrossRef
90.
go back to reference Nakagawa S, Schielzeth H. A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol Evol. 2013;4:133–42.CrossRef Nakagawa S, Schielzeth H. A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol Evol. 2013;4:133–42.CrossRef
92.
go back to reference Smith T, Charlwood JD, Takken W, Tanner M, Spiegelhalter DJ. Mapping densities of malaria vectors within a single village. Acta Trop. 1995;59:1–18.PubMedCrossRef Smith T, Charlwood JD, Takken W, Tanner M, Spiegelhalter DJ. Mapping densities of malaria vectors within a single village. Acta Trop. 1995;59:1–18.PubMedCrossRef
93.
go back to reference Magbity EB, Lines JD, Marbiah MT, David K, Peterson E. How reliable are light traps in estimating biting rates of adult Anopheles gambiae s.l. (Diptera: Culicidae) in the presence of treated bed nets? Bull Entomol Res. 2002;92:71–6.PubMedCrossRef Magbity EB, Lines JD, Marbiah MT, David K, Peterson E. How reliable are light traps in estimating biting rates of adult Anopheles gambiae s.l. (Diptera: Culicidae) in the presence of treated bed nets? Bull Entomol Res. 2002;92:71–6.PubMedCrossRef
94.
go back to reference Lindsay SW, Schellenberg JRMA, Zeiler HA, Daly RJ, Salum FM, Wilkins HA. Exposure of Gambian children to Anopheles gambiae vectors in an irrigated rice production area. Med Vet Entomol. 1995;9:50–8.PubMedCrossRef Lindsay SW, Schellenberg JRMA, Zeiler HA, Daly RJ, Salum FM, Wilkins HA. Exposure of Gambian children to Anopheles gambiae vectors in an irrigated rice production area. Med Vet Entomol. 1995;9:50–8.PubMedCrossRef
95.
go back to reference Mwakitalu ME, Malecela MN, Pedersen EM, Mosha FW, Simonsen PE. Urban lymphatic filariasis in the metropolis of Dar es Salaam, Tanzania. Parasit Vectors. 2013;6:286.PubMedPubMedCentralCrossRef Mwakitalu ME, Malecela MN, Pedersen EM, Mosha FW, Simonsen PE. Urban lymphatic filariasis in the metropolis of Dar es Salaam, Tanzania. Parasit Vectors. 2013;6:286.PubMedPubMedCentralCrossRef
96.
go back to reference MacDonald G. The epidemiology and control of malaria. London: Oxford University Press; 1957. MacDonald G. The epidemiology and control of malaria. London: Oxford University Press; 1957.
97.
go back to reference Garrett-Jones C, Shidrawi GR. Malaria vectorial capacity of a population of Anopheles gambiae. Bull World Health Organ. 1969;40:531–45.PubMedPubMedCentral Garrett-Jones C, Shidrawi GR. Malaria vectorial capacity of a population of Anopheles gambiae. Bull World Health Organ. 1969;40:531–45.PubMedPubMedCentral
98.
go back to reference Takken W, Verhulst NO. Host preferences of blood-feeding mosquitoes. Annu Rev Entomol. 2013;58:433–53.PubMedCrossRef Takken W, Verhulst NO. Host preferences of blood-feeding mosquitoes. Annu Rev Entomol. 2013;58:433–53.PubMedCrossRef
99.
go back to reference Lyimo IN, Ferguson HM. Ecological and evolutionary determinants of host species choice in mosquito vectors. Trends Parasitol. 2009;25:189–96.PubMedCrossRef Lyimo IN, Ferguson HM. Ecological and evolutionary determinants of host species choice in mosquito vectors. Trends Parasitol. 2009;25:189–96.PubMedCrossRef
100.
go back to reference Lefevre T, Gouagna LC, Dabire KR, Elguero E, Fontenille D, Renaud F, et al. Beyond nature and nurture: phenotypic plasticity in blood-feeding behavior of Anopheles gambiae s.s. when humans are not readily accessible. Am J Trop Med Hyg. 2009;81:1023–9.PubMedCrossRef Lefevre T, Gouagna LC, Dabire KR, Elguero E, Fontenille D, Renaud F, et al. Beyond nature and nurture: phenotypic plasticity in blood-feeding behavior of Anopheles gambiae s.s. when humans are not readily accessible. Am J Trop Med Hyg. 2009;81:1023–9.PubMedCrossRef
101.
go back to reference Kiszewski A, Mellinger A, Spielman A, Malaney P, Sachs SE, Sachs J, et al. A global index representing the stability of malaria transmission. Am J Trop Med Hyg. 2004;70:486–98.PubMed Kiszewski A, Mellinger A, Spielman A, Malaney P, Sachs SE, Sachs J, et al. A global index representing the stability of malaria transmission. Am J Trop Med Hyg. 2004;70:486–98.PubMed
102.
go back to reference Mayagaya VS, Nkwengulila G, Lyimo I, Kihonda J, Mtambala H. The impact of livestock on the abundance, resting behaviour and sporozoite rate of malaria vectors in southern Tanzania. Malar J. 2015;14:17.PubMedPubMedCentralCrossRef Mayagaya VS, Nkwengulila G, Lyimo I, Kihonda J, Mtambala H. The impact of livestock on the abundance, resting behaviour and sporozoite rate of malaria vectors in southern Tanzania. Malar J. 2015;14:17.PubMedPubMedCentralCrossRef
103.
go back to reference Kay BH, Boreham PFL, Edman JD. Application of the “feeding index” concept to studies of mosquito host-feeding patterns. Mosq News. 1979;39:68–73. Kay BH, Boreham PFL, Edman JD. Application of the “feeding index” concept to studies of mosquito host-feeding patterns. Mosq News. 1979;39:68–73.
104.
go back to reference Killeen GF, McKenzie FE, Foy BD, Bogh C, Beier JC. The availability of potential hosts as a determinant of feeding behaviours and malaria transmission by mosquito populations. Trans R SocTrop Med Hyg. 2001;95:469–76.CrossRef Killeen GF, McKenzie FE, Foy BD, Bogh C, Beier JC. The availability of potential hosts as a determinant of feeding behaviours and malaria transmission by mosquito populations. Trans R SocTrop Med Hyg. 2001;95:469–76.CrossRef
105.
go back to reference Garrett-Jones C. The human blood index of malarial vectors in relationship to epidemiological assessment. Bull World Health Organ. 1964;30:241–61.PubMedPubMedCentral Garrett-Jones C. The human blood index of malarial vectors in relationship to epidemiological assessment. Bull World Health Organ. 1964;30:241–61.PubMedPubMedCentral
106.
go back to reference Detinova TS, Gillies MT. Observations on the determination of the age composition and epidemiological importance of populations of Anopheles gambiae Giles and Anopheles funestus Giles in Tanganyika. Bull World Health Org. 1964;30:23–8.PubMedPubMedCentral Detinova TS, Gillies MT. Observations on the determination of the age composition and epidemiological importance of populations of Anopheles gambiae Giles and Anopheles funestus Giles in Tanganyika. Bull World Health Org. 1964;30:23–8.PubMedPubMedCentral
107.
go back to reference Detinova TS. Age-grouping methods in diptera of medical importance, with special reference to some vectors of malaria. Geneva: World Health Organization; 1962. Detinova TS. Age-grouping methods in diptera of medical importance, with special reference to some vectors of malaria. Geneva: World Health Organization; 1962.
108.
go back to reference Charlwood JD, Wilkes TJ. Studies on the age composition of sample of Anopheles darlingi Root (Diptera: culicidae) in Brazil. Bull Entomol Res. 1979;69:337–42.CrossRef Charlwood JD, Wilkes TJ. Studies on the age composition of sample of Anopheles darlingi Root (Diptera: culicidae) in Brazil. Bull Entomol Res. 1979;69:337–42.CrossRef
109.
go back to reference Mayagaya VS, Michel K, Benedict MQ, Killeen GF, Wirtz RA, Ferguson HM, et al. Non-destructive determination of age and species of Anopheles gambiae s.l. using near-infrared spectroscopy. Am J Trop Med Hyg. 2009;81:622–30.PubMedCrossRef Mayagaya VS, Michel K, Benedict MQ, Killeen GF, Wirtz RA, Ferguson HM, et al. Non-destructive determination of age and species of Anopheles gambiae s.l. using near-infrared spectroscopy. Am J Trop Med Hyg. 2009;81:622–30.PubMedCrossRef
110.
go back to reference Sikulu M, Killeen GF, Hugo LE, Ryan PA, Dowell KM, Wirtz RA, et al. Near-infrared spectroscopy as a complementary age grading and species identification tool for African malaria vectors. Parasit Vectors. 2010;3:49.PubMedPubMedCentralCrossRef Sikulu M, Killeen GF, Hugo LE, Ryan PA, Dowell KM, Wirtz RA, et al. Near-infrared spectroscopy as a complementary age grading and species identification tool for African malaria vectors. Parasit Vectors. 2010;3:49.PubMedPubMedCentralCrossRef
111.
go back to reference Dowell FE, Noutcha AEM, Michel K. The effect of preservation methods on predicting mosquito age by near infrared spectroscopy. Am J Trop Med Hyg. 2011;85:1092–6.CrossRef Dowell FE, Noutcha AEM, Michel K. The effect of preservation methods on predicting mosquito age by near infrared spectroscopy. Am J Trop Med Hyg. 2011;85:1092–6.CrossRef
112.
go back to reference Yohannes M, Boelee E. Early biting rhythm in the Afro-tropical vector of malaria, Anopheles arabiensis and challenges for its control in Ethiopia. Med Vet Entomol. 2012;26:103–5.PubMedCrossRef Yohannes M, Boelee E. Early biting rhythm in the Afro-tropical vector of malaria, Anopheles arabiensis and challenges for its control in Ethiopia. Med Vet Entomol. 2012;26:103–5.PubMedCrossRef
Metadata
Title
An improved mosquito electrocuting trap that safely reproduces epidemiologically relevant metrics of mosquito human-feeding behaviours as determined by human landing catch
Authors
Nicodem J. Govella
Deodatus F. Maliti
Amos T. Mlwale
John P. Masallu
Nosrat Mirzai
Paul C. D. Johnson
Heather M. Ferguson
Gerry F. Killeen
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/s12936-016-1513-1

Other articles of this Issue 1/2016

Malaria Journal 1/2016 Go to the issue