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Published in: Malaria Journal 1/2017

Open Access 01-12-2017 | Research

Is outdoor vector control needed for malaria elimination? An individual-based modelling study

Authors: Lin Zhu, Günter C. Müller, John M. Marshall, Kristopher L. Arheart, Whitney A. Qualls, WayWay M. Hlaing, Yosef Schlein, Sekou F. Traore, Seydou Doumbia, John C. Beier

Published in: Malaria Journal | Issue 1/2017

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Abstract

Background

Residual malaria transmission has been reported in many areas even with adequate indoor vector control coverage, such as long-lasting insecticidal nets (LLINs). The increased insecticide resistance in Anopheles mosquitoes has resulted in reduced efficacy of the widely used indoor tools and has been linked with an increase in outdoor malaria transmission. There are considerations of incorporating outdoor interventions into integrated vector management (IVM) to achieve malaria elimination; however, more information on the combination of tools for effective control is needed to determine their utilization.

Methods

A spatial individual-based model was modified to simulate the environment and malaria transmission activities in a hypothetical, isolated African village setting. LLINs and outdoor attractive toxic sugar bait (ATSB) stations were used as examples of indoor and outdoor interventions, respectively. Different interventions and lengths of efficacy periods were tested. Simulations continued for 420 days, and each simulation scenario was repeated 50 times. Mosquito populations, entomologic inoculation rates (EIRs), probabilities of local mosquito extinction, and proportion of time when the annual EIR was reduced below one were compared between different intervention types and efficacy periods.

Results

In the village setting with clustered houses, the combinational intervention of 50% LLINs plus outdoor ATSBs significantly reduced mosquito population and EIR in short term, increased the probability of local mosquito extinction, and increased the time when annual EIR is less than one per person compared to 50% LLINs alone; outdoor ATSBs alone significantly reduced mosquito population in short term, increased the probability of mosquito extinction, and increased the time when annual EIR is less than one compared to 50% LLINs alone, but there was no significant difference in EIR in short term between 50% LLINs and outdoor ATSBs. In the village setting with dispersed houses, the combinational intervention of 50% LLINs plus outdoor ATSBs significantly reduced mosquito population in short term, increased the probability of mosquito extinction, and increased the time when annual EIR is less than one per person compared to 50% LLINs alone; outdoor ATSBs alone significantly reduced mosquito population in short term, but there were no significant difference in the probability of mosquito extinction and the time when annual EIR is less than one between 50% LLIN and outdoor ATSBs; and there was no significant difference in EIR between all three interventions. A minimum of 2 months of efficacy period is needed to bring out the best possible effect of the vector control tools, and to achieve long-term mosquito reduction, a minimum of 3 months of efficacy period is needed.

Conclusions

The results highlight the value of incorporating outdoor vector control into IVM as a supplement to traditional indoor practices for malaria elimination in Africa, especially in village settings of clustered houses where LLINs alone is far from sufficient.
Literature
1.
go back to reference Mabaso ML, 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.CrossRefPubMed Mabaso ML, 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.CrossRefPubMed
2.
go back to reference Sharp BL, Kleinschmidt I, Streat E, Maharaj R, Barnes KI, Durrheim DN, et al. Seven years of regional malaria control collaboration—Mozambique, South Africa, and Swaziland. Am J Trop Med Hyg. 2007;76:42–7.PubMedPubMedCentral Sharp BL, Kleinschmidt I, Streat E, Maharaj R, Barnes KI, Durrheim DN, et al. Seven years of regional malaria control collaboration—Mozambique, South Africa, and Swaziland. Am J Trop Med Hyg. 2007;76:42–7.PubMedPubMedCentral
3.
go back to reference Kleinschmidt I, Schwabe C, Benavente L, Torrez M, Ridl FC, Segura JL, et al. Marked increase in child survival after four years of intensive malaria control. Am J Trop Med Hyg. 2009;80:882–8.PubMedPubMedCentral Kleinschmidt I, Schwabe C, Benavente L, Torrez M, Ridl FC, Segura JL, et al. Marked increase in child survival after four years of intensive malaria control. Am J Trop Med Hyg. 2009;80:882–8.PubMedPubMedCentral
4.
go back to reference Chizema-Kawesha E, Miller JM, Steketee RW, Mukonka VM, Mukuka C, Mohamed AD, et al. Scaling up malaria control in Zambia: progress and impact 2005–2008. Am J Trop Med Hyg. 2010;83:480–8.CrossRefPubMedPubMedCentral Chizema-Kawesha E, Miller JM, Steketee RW, Mukonka VM, Mukuka C, Mohamed AD, et al. Scaling up malaria control in Zambia: progress and impact 2005–2008. Am J Trop Med Hyg. 2010;83:480–8.CrossRefPubMedPubMedCentral
5.
7.
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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
8.
go back to reference N’Guessan R, Corbel V, Akogbéto M, Rowland M. Reduced efficacy of insecticide-treated nets and indoor residual spraying for malaria control in pyrethroid resistance area, Benin. Emerg Infect Dis. 2007;13:199.CrossRefPubMedPubMedCentral N’Guessan R, Corbel V, Akogbéto M, Rowland M. Reduced efficacy of insecticide-treated nets and indoor residual spraying for malaria control in pyrethroid resistance area, Benin. Emerg Infect Dis. 2007;13:199.CrossRefPubMedPubMedCentral
9.
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.CrossRefPubMed 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.CrossRefPubMed
10.
go back to reference Padonou GG, Sezonlin M, Ossé R, Aizoun N, Oké-Agbo F, Oussou O, et al. Impact of three years of large scale Indoor Residual Spraying (IRS) and Insecticide Treated Nets (ITNs) interventions on insecticide resistance in Anopheles gambiae s.l. in Benin. Parasit Vectors. 2012;5:72.CrossRefPubMedPubMedCentral Padonou GG, Sezonlin M, Ossé R, Aizoun N, Oké-Agbo F, Oussou O, et al. Impact of three years of large scale Indoor Residual Spraying (IRS) and Insecticide Treated Nets (ITNs) interventions on insecticide resistance in Anopheles gambiae s.l. in Benin. Parasit Vectors. 2012;5:72.CrossRefPubMedPubMedCentral
11.
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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
12.
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.CrossRefPubMed 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.CrossRefPubMed
13.
14.
go back to reference Sougoufara S, Diédhiou SM, Doucouré S, Diagne N, Sembène PM, Harry M, et al. Biting by Anopheles funestus in broad daylight after use of long-lasting insecticidal nets: a new challenge to malaria elimination. Malar J. 2014;13:125.CrossRefPubMedPubMedCentral Sougoufara S, Diédhiou SM, Doucouré S, Diagne N, Sembène PM, Harry M, et al. Biting by Anopheles funestus in broad daylight after use of long-lasting insecticidal nets: a new challenge to malaria elimination. Malar J. 2014;13:125.CrossRefPubMedPubMedCentral
15.
go back to reference Russell TL, Beebe NW, Bugoro H, Apairamo A, Chow WK, Cooper RD, et al. Frequent blood feeding enables insecticide-treated nets to reduce transmission by mosquitoes that bite predominately outdoors. Malar J. 2016;15:156.CrossRefPubMedPubMedCentral Russell TL, Beebe NW, Bugoro H, Apairamo A, Chow WK, Cooper RD, et al. Frequent blood feeding enables insecticide-treated nets to reduce transmission by mosquitoes that bite predominately outdoors. Malar J. 2016;15:156.CrossRefPubMedPubMedCentral
16.
go back to reference Ndenga BA, Mulaya NL, Musaki SK, Shiroko JN, Dongus S, Fillinger U. Malaria vectors and their blood-meal sources in an area of high bed net ownership in the western Kenya highlands. Malar J. 2016;15:1.CrossRef Ndenga BA, Mulaya NL, Musaki SK, Shiroko JN, Dongus S, Fillinger U. Malaria vectors and their blood-meal sources in an area of high bed net ownership in the western Kenya highlands. Malar J. 2016;15:1.CrossRef
17.
go back to reference Killeen GF, Govella NJ, Lwetoijera DW, Okumu FO. Most outdoor malaria transmission by behaviourally-resistant Anopheles arabiensis is mediated by mosquitoes that have previously been inside houses. Malar J. 2016;15:76.CrossRef Killeen GF, Govella NJ, Lwetoijera DW, Okumu FO. Most outdoor malaria transmission by behaviourally-resistant Anopheles arabiensis is mediated by mosquitoes that have previously been inside houses. Malar J. 2016;15:76.CrossRef
18.
go back to reference Govella NJ, Ferguson H. Why use of interventions targeting outdoor biting mosquitoes will be necessary to achieve malaria elimination. Front Physiol. 2012;3:199.CrossRefPubMedPubMedCentral Govella NJ, Ferguson H. Why use of interventions targeting outdoor biting mosquitoes will be necessary to achieve malaria elimination. Front Physiol. 2012;3:199.CrossRefPubMedPubMedCentral
19.
go back to reference Bugoro H, Cooper RD, Butafa C, Iro’ofa C, Mackenzie DO, Chen C-C, Russell TL. Bionomics of the malaria vector Anopheles farauti in Temotu Province, Solomon Islands: issues for malaria elimination. Malar J. 2011;10:133.CrossRefPubMedPubMedCentral Bugoro H, Cooper RD, Butafa C, Iro’ofa C, Mackenzie DO, Chen C-C, Russell TL. Bionomics of the malaria vector Anopheles farauti in Temotu Province, Solomon Islands: issues for malaria elimination. Malar J. 2011;10:133.CrossRefPubMedPubMedCentral
20.
go back to reference Monroe A, Asamoah O, Lam Y, Koenker H, Psychas P, Lynch M, et al. Outdoor-sleeping and other night-time activities in northern Ghana: implications for residual transmission and malaria prevention. Malar J. 2015;14:35.CrossRefPubMedPubMedCentral Monroe A, Asamoah O, Lam Y, Koenker H, Psychas P, Lynch M, et al. Outdoor-sleeping and other night-time activities in northern Ghana: implications for residual transmission and malaria prevention. Malar J. 2015;14:35.CrossRefPubMedPubMedCentral
21.
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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
22.
go back to reference Xue R-D, Smith ML, Qualls WA. Field evaluation of truck-mounted thermal fog of DUET™ and Aqualuer® using different solvents against Aedes albopictus. J Am Mosq Control Assoc. 2013;29:301–3.CrossRefPubMed Xue R-D, Smith ML, Qualls WA. Field evaluation of truck-mounted thermal fog of DUET™ and Aqualuer® using different solvents against Aedes albopictus. J Am Mosq Control Assoc. 2013;29:301–3.CrossRefPubMed
23.
go back to reference Fulcher A, Farooq M, Richardson AG, Smith ML, Scott JM, Gaines MK, Xue R-D. Characteristics and efficacy of three commercial handheld thermal foggers with pyrethroid insecticides against three species of mosquitoes. J Am Mosq Control Assoc. 2016;32:44–50.CrossRefPubMed Fulcher A, Farooq M, Richardson AG, Smith ML, Scott JM, Gaines MK, Xue R-D. Characteristics and efficacy of three commercial handheld thermal foggers with pyrethroid insecticides against three species of mosquitoes. J Am Mosq Control Assoc. 2016;32:44–50.CrossRefPubMed
24.
go back to reference Rowland M, Durrani N, Kenward M, Mohammed N, Urahman H, Hewitt S. Control of malaria in Pakistan by applying deltamethrin insecticide to cattle: a community-randomised trial. Lancet. 2001;357:1837–41.CrossRefPubMed Rowland M, Durrani N, Kenward M, Mohammed N, Urahman H, Hewitt S. Control of malaria in Pakistan by applying deltamethrin insecticide to cattle: a community-randomised trial. Lancet. 2001;357:1837–41.CrossRefPubMed
25.
go back to reference Chaccour CJ, Kobylinski KC, Bassat Q, Bousema T, Drakeley C, Alonso P, et al. Ivermectin to reduce malaria transmission: a research agenda for a promising new tool for elimination. Malar J. 2013;12:153.CrossRefPubMedPubMedCentral Chaccour CJ, Kobylinski KC, Bassat Q, Bousema T, Drakeley C, Alonso P, et al. Ivermectin to reduce malaria transmission: a research agenda for a promising new tool for elimination. Malar J. 2013;12:153.CrossRefPubMedPubMedCentral
26.
go back to reference Poché RM, Burruss D, Polyakova L, Poché DM, Garlapati RB. Treatment of livestock with systemic insecticides for control of Anopheles arabiensis in western Kenya. Malar J. 2015;14:351.CrossRefPubMedPubMedCentral Poché RM, Burruss D, Polyakova L, Poché DM, Garlapati RB. Treatment of livestock with systemic insecticides for control of Anopheles arabiensis in western Kenya. Malar J. 2015;14:351.CrossRefPubMedPubMedCentral
28.
go back to reference Wagman JM, Grieco JP, Bautista K, Polanco J, Briceño I, King R, Achee NL. The field evaluation of a push–pull system to control malaria vectors in Northern Belize, Central America. Malar J. 2015;14:184.CrossRefPubMedPubMedCentral Wagman JM, Grieco JP, Bautista K, Polanco J, Briceño I, King R, Achee NL. The field evaluation of a push–pull system to control malaria vectors in Northern Belize, Central America. Malar J. 2015;14:184.CrossRefPubMedPubMedCentral
29.
go back to reference Menger DJ, Omusula P, Wouters K, Oketch C, Carreira AS, Durka M, et al. Eave screening and push–pull tactics to reduce house entry by vectors of malaria. Am J Trop Med Hyg. 2016;94:868–78.CrossRefPubMedPubMedCentral Menger DJ, Omusula P, Wouters K, Oketch C, Carreira AS, Durka M, et al. Eave screening and push–pull tactics to reduce house entry by vectors of malaria. Am J Trop Med Hyg. 2016;94:868–78.CrossRefPubMedPubMedCentral
30.
go back to reference Matowo NS, Koekemoer LL, Moore SJ, Mmbando AS, Mapua SA, Coetzee M, et al. Combining synthetic human odours and low-cost electrocuting grids to attract and kill outdoor-biting mosquitoes: field and semi-field evaluation of an improved mosquito landing box. PLoS ONE. 2016;11:e0145653.CrossRefPubMedPubMedCentral Matowo NS, Koekemoer LL, Moore SJ, Mmbando AS, Mapua SA, Coetzee M, et al. Combining synthetic human odours and low-cost electrocuting grids to attract and kill outdoor-biting mosquitoes: field and semi-field evaluation of an improved mosquito landing box. PLoS ONE. 2016;11:e0145653.CrossRefPubMedPubMedCentral
31.
go back to reference Mmbando AS, Okumu FO, Mgando JP, Sumaye RD, Matowo NS, Madumla E, et al. Effects of a new outdoor mosquito control device, the mosquito landing box, on densities and survival of the malaria vector, Anopheles arabiensis, inside controlled semi-field settings. Malar J. 2015;14:494.CrossRefPubMedPubMedCentral Mmbando AS, Okumu FO, Mgando JP, Sumaye RD, Matowo NS, Madumla E, et al. Effects of a new outdoor mosquito control device, the mosquito landing box, on densities and survival of the malaria vector, Anopheles arabiensis, inside controlled semi-field settings. Malar J. 2015;14:494.CrossRefPubMedPubMedCentral
32.
go back to reference Smith DL, Perkins TA, Tusting LS, Scott TW, Lindsay SW. Mosquito population regulation and larval source management in heterogeneous environments. PLoS ONE. 2013;8:e71247.CrossRefPubMedPubMedCentral Smith DL, Perkins TA, Tusting LS, Scott TW, Lindsay SW. Mosquito population regulation and larval source management in heterogeneous environments. PLoS ONE. 2013;8:e71247.CrossRefPubMedPubMedCentral
33.
go back to reference WHO. Larval source management: a supplementary malaria vector control measure: an operational manual. Geneva: World Health Organization; 2013. WHO. Larval source management: a supplementary malaria vector control measure: an operational manual. Geneva: World Health Organization; 2013.
34.
go back to reference Majambere S, Pinder M, Fillinger U, Ameh D, Conway DJ, Green C, et al. Is mosquito larval source management appropriate for reducing malaria in areas of extensive flooding in The Gambia? A cross-over intervention trial. Am J Trop Med Hyg. 2010;82:176–84.CrossRefPubMedPubMedCentral Majambere S, Pinder M, Fillinger U, Ameh D, Conway DJ, Green C, et al. Is mosquito larval source management appropriate for reducing malaria in areas of extensive flooding in The Gambia? A cross-over intervention trial. Am J Trop Med Hyg. 2010;82:176–84.CrossRefPubMedPubMedCentral
35.
go back to reference Müller GC, Kravchenko VD, Schlein Y. Decline of Anopheles sergentii and Aedes caspius populations following presentation of attractive toxic (spinosad) sugar bait stations in an oasis. J Am Mosq Control Assoc. 2008;24:147–9.CrossRefPubMed Müller GC, Kravchenko VD, Schlein Y. Decline of Anopheles sergentii and Aedes caspius populations following presentation of attractive toxic (spinosad) sugar bait stations in an oasis. J Am Mosq Control Assoc. 2008;24:147–9.CrossRefPubMed
36.
go back to reference Müller GC, Schlein Y. Efficacy of toxic sugar baits against adult cistern-dwelling Anopheles claviger. Trans R Soc Trop Med Hyg. 2008;102:480–4.CrossRefPubMed Müller GC, Schlein Y. Efficacy of toxic sugar baits against adult cistern-dwelling Anopheles claviger. Trans R Soc Trop Med Hyg. 2008;102:480–4.CrossRefPubMed
37.
38.
go back to reference Müller GC, Beier JC, Traore SF, Toure MB, Traore MM, Bah S, et al. Successful field trial of attractive toxic sugar bait (ATSB) plant-spraying methods against malaria vectors in the Anopheles gambiae complex in Mali, West Africa. Malar J. 2010;9:210.CrossRefPubMedPubMedCentral Müller GC, Beier JC, Traore SF, Toure MB, Traore MM, Bah S, et al. Successful field trial of attractive toxic sugar bait (ATSB) plant-spraying methods against malaria vectors in the Anopheles gambiae complex in Mali, West Africa. Malar J. 2010;9:210.CrossRefPubMedPubMedCentral
39.
go back to reference Beier JC, Müller GC, Gu W, Arheart KL, Schlein Y. Attractive toxic sugar bait (ATSB) methods decimate populations of Anopheles malaria vectors in arid environments regardless of the local availability of favoured sugar-source blossoms. Malar J. 2012;11:31.CrossRefPubMedPubMedCentral Beier JC, Müller GC, Gu W, Arheart KL, Schlein Y. Attractive toxic sugar bait (ATSB) methods decimate populations of Anopheles malaria vectors in arid environments regardless of the local availability of favoured sugar-source blossoms. Malar J. 2012;11:31.CrossRefPubMedPubMedCentral
40.
go back to reference Qualls WA, Müller GC, Traore SF, Traore MM, Arheart KL, Doumbia S, et al. Indoor use of attractive toxic sugar bait (ATSB) to effectively control malaria vectors in Mali, West Africa. Malar J. 2015;14:301.CrossRefPubMedPubMedCentral Qualls WA, Müller GC, Traore SF, Traore MM, Arheart KL, Doumbia S, et al. Indoor use of attractive toxic sugar bait (ATSB) to effectively control malaria vectors in Mali, West Africa. Malar J. 2015;14:301.CrossRefPubMedPubMedCentral
41.
go back to reference Zhu L, Marshall JM, Qualls WA, Schlein Y, McManus JW, Arheart KL, et al. Modelling optimum use of attractive toxic sugar bait stations for effective malaria vector control in Africa. Malar J. 2015;14:492.CrossRefPubMedPubMedCentral Zhu L, Marshall JM, Qualls WA, Schlein Y, McManus JW, Arheart KL, et al. Modelling optimum use of attractive toxic sugar bait stations for effective malaria vector control in Africa. Malar J. 2015;14:492.CrossRefPubMedPubMedCentral
42.
go back to reference Koenker H, Kilian A, de Beyl CZ, Onyefunafoa EO, Selby RA, Abeku T, et al. What happens to lost nets: a multi-country analysis of reasons for LLIN attrition using 14 household surveys in four countries. Malar J. 2014;13:464.CrossRefPubMedPubMedCentral Koenker H, Kilian A, de Beyl CZ, Onyefunafoa EO, Selby RA, Abeku T, et al. What happens to lost nets: a multi-country analysis of reasons for LLIN attrition using 14 household surveys in four countries. Malar J. 2014;13:464.CrossRefPubMedPubMedCentral
43.
go back to reference Batisso E, Habte T, Tesfaye G, Getachew D, Tekalegne A, Kilian A, et al. A stitch in time: a cross-sectional survey looking at long lasting insecticide-treated bed net ownership, utilization and attrition in SNNPR, Ethiopia. Malar J. 2012;11:183.CrossRefPubMedPubMedCentral Batisso E, Habte T, Tesfaye G, Getachew D, Tekalegne A, Kilian A, et al. A stitch in time: a cross-sectional survey looking at long lasting insecticide-treated bed net ownership, utilization and attrition in SNNPR, Ethiopia. Malar J. 2012;11:183.CrossRefPubMedPubMedCentral
44.
go back to reference Hakizimana E, Cyubahiro B, Rukundo A, Kabayiza A, Mutabazi A, Beach R, et al. Monitoring long-lasting insecticidal net (LLIN) durability to validate net serviceable life assumptions, in Rwanda. Malar J. 2014;13:344.CrossRefPubMedPubMedCentral Hakizimana E, Cyubahiro B, Rukundo A, Kabayiza A, Mutabazi A, Beach R, et al. Monitoring long-lasting insecticidal net (LLIN) durability to validate net serviceable life assumptions, in Rwanda. Malar J. 2014;13:344.CrossRefPubMedPubMedCentral
45.
go back to reference Morgan J, Abílio AP, do Rosario Pondja M, Marrenjo D, Luciano J, Fernandes G, et al. Physical durability of two types of long-lasting insecticidal nets (LLINs) three years after a mass LLIN distribution campaign in Mozambique, 2008–2011. Am J Trop Med Hyg. 2015;92:286–93.CrossRefPubMedPubMedCentral Morgan J, Abílio AP, do Rosario Pondja M, Marrenjo D, Luciano J, Fernandes G, et al. Physical durability of two types of long-lasting insecticidal nets (LLINs) three years after a mass LLIN distribution campaign in Mozambique, 2008–2011. Am J Trop Med Hyg. 2015;92:286–93.CrossRefPubMedPubMedCentral
46.
go back to reference Tan KR, Coleman J, Smith B, Hamainza B, Katebe-Sakala C, Kean C, et al. A longitudinal study of the durability of long-lasting insecticidal nets in Zambia. Malar J. 2016;15:106.CrossRefPubMedPubMedCentral Tan KR, Coleman J, Smith B, Hamainza B, Katebe-Sakala C, Kean C, et al. A longitudinal study of the durability of long-lasting insecticidal nets in Zambia. Malar J. 2016;15:106.CrossRefPubMedPubMedCentral
47.
48.
go back to reference Griffin JT, Hollingsworth TD, Okell LC, Churcher TS, White M, Hinsley W, et al. Reducing Plasmodium falciparum malaria transmission in Africa: a model-based evaluation of intervention strategies. PLoS Med. 2010;7:1000324.CrossRef Griffin JT, Hollingsworth TD, Okell LC, Churcher TS, White M, Hinsley W, et al. Reducing Plasmodium falciparum malaria transmission in Africa: a model-based evaluation of intervention strategies. PLoS Med. 2010;7:1000324.CrossRef
49.
go back to reference Marshall JM, White MT, Ghani AC, Schlein Y, Müller GC, Beier JC. Quantifying the mosquito’s sweet tooth: modelling the effectiveness of attractive toxic sugar baits (ATSB) for malaria vector control. Malar J. 2013;12:291.CrossRefPubMedPubMedCentral Marshall JM, White MT, Ghani AC, Schlein Y, Müller GC, Beier JC. Quantifying the mosquito’s sweet tooth: modelling the effectiveness of attractive toxic sugar baits (ATSB) for malaria vector control. Malar J. 2013;12:291.CrossRefPubMedPubMedCentral
50.
go back to reference Zhu L, Qualls WA, Marshall JM, Arheart KL, DeAngelis DL, McManus JW, et al. A spatial individual-based model predicting a great impact of copious sugar sources and resting sites on survival of Anopheles gambiae and malaria parasite transmission. Malar J. 2015;14:59.CrossRefPubMedPubMedCentral Zhu L, Qualls WA, Marshall JM, Arheart KL, DeAngelis DL, McManus JW, et al. A spatial individual-based model predicting a great impact of copious sugar sources and resting sites on survival of Anopheles gambiae and malaria parasite transmission. Malar J. 2015;14:59.CrossRefPubMedPubMedCentral
51.
go back to reference Okech BA, Gouagna LC, Killeen GF, Knols BG, Kabiru EW, Beier JC, et al. Influence of sugar availability and indoor microclimate on survival of Anopheles gambiae (Diptera: Culicidae) under semifield conditions in western Kenya. J Med Entomol. 2003;40:657–63.CrossRefPubMed Okech BA, Gouagna LC, Killeen GF, Knols BG, Kabiru EW, Beier JC, et al. Influence of sugar availability and indoor microclimate on survival of Anopheles gambiae (Diptera: Culicidae) under semifield conditions in western Kenya. J Med Entomol. 2003;40:657–63.CrossRefPubMed
52.
go back to reference Afrane YA, Zhou G, Lawson BW, Githeko AK, Yan G. Effects of microclimatic changes caused by deforestation on the survivorship and reproductive fitness of Anopheles gambiae in western Kenya highlands. Am J Trop Med Hyg. 2006;74:772–8.PubMed Afrane YA, Zhou G, Lawson BW, Githeko AK, Yan G. Effects of microclimatic changes caused by deforestation on the survivorship and reproductive fitness of Anopheles gambiae in western Kenya highlands. Am J Trop Med Hyg. 2006;74:772–8.PubMed
53.
go back to reference Olayemi IKA, Ande AT. Life table analysis of Anopheles gambiae (Diptera: Culicidae) in relation to malaria transmission. J Vector Borne Dis. 2009;46:295–8.PubMed Olayemi IKA, Ande AT. Life table analysis of Anopheles gambiae (Diptera: Culicidae) in relation to malaria transmission. J Vector Borne Dis. 2009;46:295–8.PubMed
54.
go back to reference Lines J, Wilkes T, Lyimo E. Human malaria infectiousness measured by age-specific sporozoite rates in Anopheles gambiae in Tanzania. Parasitology. 1991;102:167–77.CrossRefPubMed Lines J, Wilkes T, Lyimo E. Human malaria infectiousness measured by age-specific sporozoite rates in Anopheles gambiae in Tanzania. Parasitology. 1991;102:167–77.CrossRefPubMed
55.
go back to reference Gary R, Foster W. Effects of available sugar on the reproductive fitness and vectorial capacity of the malaria vector. J Med Entomol. 2001;38:22–8.CrossRefPubMed Gary R, Foster W. Effects of available sugar on the reproductive fitness and vectorial capacity of the malaria vector. J Med Entomol. 2001;38:22–8.CrossRefPubMed
56.
go back to reference Githeko A, Brandling-Bennett A, Beier M, Atieli F, Owaga M, Collins F. The reservoir of Plasmodium falciparum malaria in a holoendemic area of western Kenya. Trans R Soc Trop Med Hyg. 1992;86:355–8.CrossRefPubMed Githeko A, Brandling-Bennett A, Beier M, Atieli F, Owaga M, Collins F. The reservoir of Plasmodium falciparum malaria in a holoendemic area of western Kenya. Trans R Soc Trop Med Hyg. 1992;86:355–8.CrossRefPubMed
57.
go back to reference Shililu J, Maier W, Seitz H, Orago A. Seasonal density, sporozoite rates and entomological inoculation rates of Anopheles gambiae and Anopheles funestus in a high altitude sugarcane growing zone in western Kenya. Trop Med Int Health. 1998;3:706–10.CrossRefPubMed Shililu J, Maier W, Seitz H, Orago A. Seasonal density, sporozoite rates and entomological inoculation rates of Anopheles gambiae and Anopheles funestus in a high altitude sugarcane growing zone in western Kenya. Trop Med Int Health. 1998;3:706–10.CrossRefPubMed
58.
go back to reference Sattabongkot J, Maneechai N, Phunkitchar V, Eikarat N, Khuntirat B, Sirichaisinthop J, et al. Comparison of artificial membrane feeding with direct skin feeding to estimate the infectiousness of Plasmodium vivax gametocyte carriers to mosquitoes. Am J Trop Med Hyg. 2003;69:529–35.PubMed Sattabongkot J, Maneechai N, Phunkitchar V, Eikarat N, Khuntirat B, Sirichaisinthop J, et al. Comparison of artificial membrane feeding with direct skin feeding to estimate the infectiousness of Plasmodium vivax gametocyte carriers to mosquitoes. Am J Trop Med Hyg. 2003;69:529–35.PubMed
59.
go back to reference Drakeley C, Sutherland C, Bousema JT, Sauerwein RW, Targett GA. The epidemiology of Plasmodium falciparum gametocytes: weapons of mass dispersion. Trends Parasitol. 2006;22:424–30.CrossRefPubMed Drakeley C, Sutherland C, Bousema JT, Sauerwein RW, Targett GA. The epidemiology of Plasmodium falciparum gametocytes: weapons of mass dispersion. Trends Parasitol. 2006;22:424–30.CrossRefPubMed
60.
go back to reference Schneider P, Bousema JT, Gouagna LC, Otieno S, Van de Vegte-Bolmer M, Omar SA, et al. Submicroscopic Plasmodium falciparum gametocyte densities frequently result in mosquito infection. Am J Trop Med Hyg. 2007;76:470–4.PubMed Schneider P, Bousema JT, Gouagna LC, Otieno S, Van de Vegte-Bolmer M, Omar SA, et al. Submicroscopic Plasmodium falciparum gametocyte densities frequently result in mosquito infection. Am J Trop Med Hyg. 2007;76:470–4.PubMed
61.
go back to reference Ouédraogo AL, Bousema T, Schneider P, De Vlas SJ, Ilboudo-Sanogo E, Cuzin-Ouattara N, et al. Substantial contribution of submicroscopical Plasmodium falciparum gametocyte carriage to the infectious reservoir in an area of seasonal transmission. PLoS ONE. 2009;4:e8410.CrossRefPubMedPubMedCentral Ouédraogo AL, Bousema T, Schneider P, De Vlas SJ, Ilboudo-Sanogo E, Cuzin-Ouattara N, et al. Substantial contribution of submicroscopical Plasmodium falciparum gametocyte carriage to the infectious reservoir in an area of seasonal transmission. PLoS ONE. 2009;4:e8410.CrossRefPubMedPubMedCentral
62.
go back to reference Bousema T, Drakeley C. Epidemiology and infectivity of Plasmodium falciparum and Plasmodium vivax gametocytes in relation to malaria control and elimination. Clin Microbiol Rev. 2011;24:377–410.CrossRefPubMedPubMedCentral Bousema T, Drakeley C. Epidemiology and infectivity of Plasmodium falciparum and Plasmodium vivax gametocytes in relation to malaria control and elimination. Clin Microbiol Rev. 2011;24:377–410.CrossRefPubMedPubMedCentral
63.
go back to reference Da DF, Churcher TS, Yerbanga RS, Yaméogo B, Sangaré I, Ouedraogo JB, et al. Experimental study of the relationship between Plasmodium gametocyte density and infection success in mosquitoes; implications for the evaluation of malaria transmission-reducing interventions. Exp Parasitol. 2015;149:74–83.CrossRefPubMed Da DF, Churcher TS, Yerbanga RS, Yaméogo B, Sangaré I, Ouedraogo JB, et al. Experimental study of the relationship between Plasmodium gametocyte density and infection success in mosquitoes; implications for the evaluation of malaria transmission-reducing interventions. Exp Parasitol. 2015;149:74–83.CrossRefPubMed
64.
go back to reference Langhorne J, Ndungu FM, Sponaas A-M, Marsh K. Immunity to malaria: more questions than answers. Nat Immunol. 2008;9:725–32.CrossRefPubMed Langhorne J, Ndungu FM, Sponaas A-M, Marsh K. Immunity to malaria: more questions than answers. Nat Immunol. 2008;9:725–32.CrossRefPubMed
65.
go back to reference Ulrich JN, Naranjo DP, Alimi TO, Müller GC, Beier JC. How much vector control is needed to achieve malaria elimination? Trends Parasitol. 2013;29:104–9.CrossRefPubMedPubMedCentral Ulrich JN, Naranjo DP, Alimi TO, Müller GC, Beier JC. How much vector control is needed to achieve malaria elimination? Trends Parasitol. 2013;29:104–9.CrossRefPubMedPubMedCentral
66.
go back to reference Gillies MT, Wilkes TJ. A study of the age-composition of populations of Anopheles gambiae Giles and A. funestus Giles in North-Eastern Tanzania. Bull Entomol Res. 1965;56:237–62.CrossRefPubMed Gillies MT, Wilkes TJ. A study of the age-composition of populations of Anopheles gambiae Giles and A. funestus Giles in North-Eastern Tanzania. Bull Entomol Res. 1965;56:237–62.CrossRefPubMed
67.
go back to reference Straif SC, Beier JC. Effects of sugar availability on the blood-feeding behavior of Anopheles gambiae (Diptera: Culicidae). J Med Entomol. 1996;33:608–12.CrossRefPubMed Straif SC, Beier JC. Effects of sugar availability on the blood-feeding behavior of Anopheles gambiae (Diptera: Culicidae). J Med Entomol. 1996;33:608–12.CrossRefPubMed
68.
go back to reference Takken W, van Loon JJ, Adam W. Inhibition of host-seeking response and olfactory responsiveness in Anopheles gambiae following blood feeding. J Insect Physiol. 2001;47:303–10.CrossRefPubMed Takken W, van Loon JJ, Adam W. Inhibition of host-seeking response and olfactory responsiveness in Anopheles gambiae following blood feeding. J Insect Physiol. 2001;47:303–10.CrossRefPubMed
69.
go back to reference Gary R, Foster W. Diel timing and frequency of sugar feeding in the mosquito Anopheles gambiae, depending on sex, gonotrophic state and resource availability. Med Vet Entomol. 2006;20:308–16.CrossRefPubMed Gary R, Foster W. Diel timing and frequency of sugar feeding in the mosquito Anopheles gambiae, depending on sex, gonotrophic state and resource availability. Med Vet Entomol. 2006;20:308–16.CrossRefPubMed
70.
go back to reference WHO. World Malaria report 2015. Geneva: World Health Organization; 2015. WHO. World Malaria report 2015. Geneva: World Health Organization; 2015.
71.
go back to reference Otten M, Aregawi M, Were W, Karema C, Medin A, Bekele W, et al. Initial evidence of reduction of malaria cases and deaths in Rwanda and Ethiopia due to rapid scale-up of malaria prevention and treatment. Malar J. 2009;8:14.CrossRefPubMedPubMedCentral Otten M, Aregawi M, Were W, Karema C, Medin A, Bekele W, et al. Initial evidence of reduction of malaria cases and deaths in Rwanda and Ethiopia due to rapid scale-up of malaria prevention and treatment. Malar J. 2009;8:14.CrossRefPubMedPubMedCentral
72.
73.
go back to reference van Eijk AM, Hill J, Larsen DA, Webster J, Steketee RW, Eisele TP, et al. Coverage of intermittent preventive treatment and insecticide-treated nets for the control of malaria during pregnancy in sub-Saharan Africa: a synthesis and meta-analysis of national survey data, 2009–2011. Lancet Infect Dis. 2013;13:1029–42.CrossRefPubMed van Eijk AM, Hill J, Larsen DA, Webster J, Steketee RW, Eisele TP, et al. Coverage of intermittent preventive treatment and insecticide-treated nets for the control of malaria during pregnancy in sub-Saharan Africa: a synthesis and meta-analysis of national survey data, 2009–2011. Lancet Infect Dis. 2013;13:1029–42.CrossRefPubMed
74.
go back to reference Ouattara AF, Dagnogo M, Constant EA, Koné M, Raso G, Tanner M, et al. Transmission of malaria in relation to distribution and coverage of long-lasting insecticidal nets in central Côte d’Ivoire. Malar J. 2014;13:109.CrossRefPubMedPubMedCentral Ouattara AF, Dagnogo M, Constant EA, Koné M, Raso G, Tanner M, et al. Transmission of malaria in relation to distribution and coverage of long-lasting insecticidal nets in central Côte d’Ivoire. Malar J. 2014;13:109.CrossRefPubMedPubMedCentral
75.
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:e309.CrossRefPubMedPubMedCentral 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:e309.CrossRefPubMedPubMedCentral
76.
go back to reference Corbel V, Akogbeto M, Damien GB, Djenontin A, Chandre F, Rogier C, et al. Combination of malaria vector control interventions in pyrethroid resistance area in Benin: a cluster randomised controlled trial. Lancet Infect Dis. 2012;12:617–26.CrossRefPubMed Corbel V, Akogbeto M, Damien GB, Djenontin A, Chandre F, Rogier C, et al. Combination of malaria vector control interventions in pyrethroid resistance area in Benin: a cluster randomised controlled trial. Lancet Infect Dis. 2012;12:617–26.CrossRefPubMed
77.
go back to reference Ross R. Studies on malaria. London: John Murray; 1928. Ross R. Studies on malaria. London: John Murray; 1928.
78.
go back to reference McKenzie FE, Killeen GF, Beier JC, Bossert WH. Seasonality, parasite diversity, and local extinctions in Plasmodium falciparum malaria. Ecology. 2001;82:2673–81.CrossRefPubMedPubMedCentral McKenzie FE, Killeen GF, Beier JC, Bossert WH. Seasonality, parasite diversity, and local extinctions in Plasmodium falciparum malaria. Ecology. 2001;82:2673–81.CrossRefPubMedPubMedCentral
79.
go back to reference Kligler I. Flight of anopheles mosquitoes. Trans R Soc Trop Med Hyg. 1924;18:199–202.CrossRef Kligler I. Flight of anopheles mosquitoes. Trans R Soc Trop Med Hyg. 1924;18:199–202.CrossRef
Metadata
Title
Is outdoor vector control needed for malaria elimination? An individual-based modelling study
Authors
Lin Zhu
Günter C. Müller
John M. Marshall
Kristopher L. Arheart
Whitney A. Qualls
WayWay M. Hlaing
Yosef Schlein
Sekou F. Traore
Seydou Doumbia
John C. Beier
Publication date
01-12-2017
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2017
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-017-1920-y

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