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

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, 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

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.

Keywords: ATSB; Agent-based model; Anopheles gambiae; Individual-based model; LLIN; Malaria elimination; Outdoor vector control; Residual malaria transmission.

Figures

Fig. 1
Fig. 1
Dynamics of female mosquito population with different intervention types and efficacy periods in clustered and dispersed village settings. The two columns of figures show the dynamics of female mosquito populations in village setting of clustered houses (on the left) and dispersed houses (on the right). The first row of figures shows results of 50% LLIN intervention, the second row shows results of outdoor ATSB intervention, and the third row shows results of 50% LLIN plus ATSB intervention. In all six figures, the y-axis represents the mean number of female An. gambiae mosquitoes at each day, and the x-axis shows the time in days. Day 0 is the day that the intervention was applied. The lines in different colors represent different simulated efficacy periods for each intervention

References

    1. 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;9:846–856. doi: 10.1111/j.1365-3156.2004.01263.x.
    1. 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;76:42–47.
    1. 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;80:882–888.
    1. 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;83:480–488. doi: 10.4269/ajtmh.2010.10-0035.
    1. Steketee RW, Campbell CC. Impact of national malaria control scale-up programmes in Africa: magnitude and attribution of effects. Malar J. 2010;9:299. doi: 10.1186/1475-2875-9-299.
    1. Killeen GF. Characterizing, controlling and eliminating residual malaria transmission. Malar J. 2014;13:330. doi: 10.1186/1475-2875-13-330.
    1. 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. doi: 10.1186/1475-2875-10-80.
    1. 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. doi: 10.3201/eid1302.060631.
    1. 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;27:91–98. doi: 10.1016/j.pt.2010.08.004.
    1. 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. doi: 10.1186/1756-3305-5-72.
    1. 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. doi: 10.1186/1475-2875-10-184.
    1. 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;206:1622–1629. doi: 10.1093/infdis/jis565.
    1. Durnez L, Mao S, Denis L, Roelants P, Sochantha T, Coosemans M. Outdoor malaria transmission in forested villages of Cambodia. Malar J. 2013;12:329. doi: 10.1186/1475-2875-12-329.
    1. 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. doi: 10.1186/1475-2875-13-125.
    1. 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. doi: 10.1186/s12936-016-1195-8.
    1. 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. doi: 10.1186/s12936-016-1115-y.
    1. 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. doi: 10.1186/s12936-016-1280-z.
    1. Govella NJ, Ferguson H. Why use of interventions targeting outdoor biting mosquitoes will be necessary to achieve malaria elimination. Front Physiol. 2012;3:199. doi: 10.3389/fphys.2012.00199.
    1. 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. doi: 10.1186/1475-2875-10-133.
    1. 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. doi: 10.1186/s12936-015-0543-4.
    1. 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. doi: 10.1186/s12936-016-1286-6.
    1. 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;29:301–303. doi: 10.2987/13-6329R.1.
    1. 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. doi: 10.2987/8756-971X-32.1.44.
    1. 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;357:1837–1841. doi: 10.1016/S0140-6736(00)04955-2.
    1. 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. doi: 10.1186/1475-2875-12-153.
    1. 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. doi: 10.1186/s12936-015-0883-0.
    1. Diabate A, Tripet F. Targeting male mosquito mating behaviour for malaria control. Parasit Vectors. 2015;8:347. doi: 10.1186/s13071-015-0961-8.
    1. 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. doi: 10.1186/s12936-015-0692-5.
    1. 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;94:868–878. doi: 10.4269/ajtmh.15-0632.
    1. 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. doi: 10.1371/journal.pone.0145653.
    1. 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. doi: 10.1186/s12936-015-1013-8.
    1. 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. doi: 10.1371/journal.pone.0071247.
    1. WHO . Larval source management: a supplementary malaria vector control measure: an operational manual. Geneva: World Health Organization; 2013.
    1. 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;82:176–184. doi: 10.4269/ajtmh.2010.09-0373.
    1. 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;24:147–149. doi: 10.2987/8756-971X(2008)24[147:DOASAA];2.
    1. Müller GC, Schlein Y. Efficacy of toxic sugar baits against adult cistern-dwelling Anopheles claviger. Trans R Soc Trop Med Hyg. 2008;102:480–484. doi: 10.1016/j.trstmh.2008.01.008.
    1. Foster WA. Mosquito sugar feeding and reproductive energetics. Annu Rev Entomol. 1995;40:443–474. doi: 10.1146/annurev.en.40.010195.002303.
    1. 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. doi: 10.1186/1475-2875-9-210.
    1. 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. doi: 10.1186/1475-2875-11-31.
    1. 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. doi: 10.1186/s12936-015-0819-8.
    1. 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. doi: 10.1186/s12936-015-1012-9.
    1. 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. doi: 10.1186/1475-2875-13-464.
    1. 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. doi: 10.1186/1475-2875-11-183.
    1. 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. doi: 10.1186/1475-2875-13-344.
    1. 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;92:286–293. doi: 10.4269/ajtmh.14-0023.
    1. 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. doi: 10.1186/s12936-016-1154-4.
    1. Beier JC, Keating J, Githure JI, Macdonald MB, Impoinvil DE, Novak RJ. Integrated vector management for malaria control. Malar J. 2008;7(Suppl 1):S4. doi: 10.1186/1475-2875-7-S1-S4.
    1. 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. doi: 10.1371/journal.pmed.1000324.
    1. 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. doi: 10.1186/1475-2875-12-291.
    1. 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. doi: 10.1186/s12936-015-0555-0.
    1. 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;40:657–663. doi: 10.1603/0022-2585-40.5.657.
    1. 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;74:772–778.
    1. Olayemi IKA, Ande AT. Life table analysis of Anopheles gambiae (Diptera: Culicidae) in relation to malaria transmission. J Vector Borne Dis. 2009;46:295–298.
    1. Lines J, Wilkes T, Lyimo E. Human malaria infectiousness measured by age-specific sporozoite rates in Anopheles gambiae in Tanzania. Parasitology. 1991;102:167–177. doi: 10.1017/S0031182000062454.
    1. Gary R, Foster W. Effects of available sugar on the reproductive fitness and vectorial capacity of the malaria vector. J Med Entomol. 2001;38:22–28. doi: 10.1603/0022-2585-38.1.22.
    1. 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;86:355–358. doi: 10.1016/0035-9203(92)90216-Y.
    1. 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;3:706–710. doi: 10.1046/j.1365-3156.1998.00282.x.
    1. 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;69:529–535.
    1. Drakeley C, Sutherland C, Bousema JT, Sauerwein RW, Targett GA. The epidemiology of Plasmodium falciparum gametocytes: weapons of mass dispersion. Trends Parasitol. 2006;22:424–430. doi: 10.1016/j.pt.2006.07.001.
    1. 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;76:470–474.
    1. 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. doi: 10.1371/journal.pone.0008410.
    1. 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. doi: 10.1128/CMR.00051-10.
    1. 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. doi: 10.1016/j.exppara.2014.12.010.
    1. Langhorne J, Ndungu FM, Sponaas A-M, Marsh K. Immunity to malaria: more questions than answers. Nat Immunol. 2008;9:725–732. doi: 10.1038/ni.f.205.
    1. Ulrich JN, Naranjo DP, Alimi TO, Müller GC, Beier JC. How much vector control is needed to achieve malaria elimination? Trends Parasitol. 2013;29:104–109. doi: 10.1016/j.pt.2013.01.002.
    1. 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;56:237–262. doi: 10.1017/S0007485300056339.
    1. Straif SC, Beier JC. Effects of sugar availability on the blood-feeding behavior of Anopheles gambiae (Diptera: Culicidae) J Med Entomol. 1996;33:608–612. doi: 10.1093/jmedent/33.4.608.
    1. 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;47:303–310. doi: 10.1016/S0022-1910(00)00107-4.
    1. 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;20:308–316. doi: 10.1111/j.1365-2915.2006.00638.x.
    1. WHO . World Malaria report 2015. Geneva: World Health Organization; 2015.
    1. 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. doi: 10.1186/1475-2875-8-14.
    1. Okiro EA, Alegana VA, Noor AM, Snow RW. Changing malaria intervention coverage, transmission and hospitalization in Kenya. Malar J. 2010;9:285. doi: 10.1186/1475-2875-9-285.
    1. 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;13:1029–1042. doi: 10.1016/S1473-3099(13)70199-3.
    1. 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. doi: 10.1186/1475-2875-13-109.
    1. 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. doi: 10.1371/journal.pmed.0040309.
    1. 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;12:617–626. doi: 10.1016/S1473-3099(12)70081-6.
    1. Ross R. Studies on malaria. London: John Murray; 1928.
    1. McKenzie FE, Killeen GF, Beier JC, Bossert WH. Seasonality, parasite diversity, and local extinctions in Plasmodium falciparum malaria. Ecology. 2001;82:2673–2681. doi: 10.2307/2679952.
    1. Kligler I. Flight of anopheles mosquitoes. Trans R Soc Trop Med Hyg. 1924;18:199–202. doi: 10.1016/S0035-9203(24)90848-0.

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