Skip to main content
Top
Published in: Malaria Journal 1/2019

Open Access 01-12-2019 | Malaria | Research

Synergy and timing: a concurrent mass medical campaign predicted to augment indoor residual spraying for malaria

Authors: Richard C. Elliott, David L. Smith, Dorothy C. Echodu

Published in: Malaria Journal | Issue 1/2019

Login to get access

Abstract

Background

Control programmes for high burden countries are tasked with charting effective multi-year strategies for malaria control within significant resource constraints. Synergies between different control tools, in which more than additive benefit accrues from interventions used together, are of interest because they may be used to obtain savings or to maximize health impact per expenditure. One commonly used intervention in sub-Saharan Africa is indoor residual spraying (IRS), typically deployed through a mass campaign. While possible synergies between IRS and long-lasting insecticide-treated nets (LLINs) have been investigated in multiple transmission settings, coordinated synergy between IRS and other mass medical distribution campaigns have not attracted much attention. Recently, a strong timing-dependent synergy between an IRS campaign and a mass drug administration (MDA) was theoretically quantified. These synergistic benefits likely differ across settings depending on transmission intensity and its overall seasonal pattern.

Methods

High coverage interventions are modelled in different transmission environments using two methods: a Ross–Macdonald model variant and openmalaria simulations. The impact of each intervention strategy was measured through its ability to prevent host infections over time, and the effects were compared to the baseline case of deploying interventions in isolation.

Results

By modelling IRS and MDA together and varying their deployment times, a strong synergy was found when the administered interventions overlapped. The added benefit of co-timed interventions was robust to differences in the models. In the Ross–Macdonald model, the impact compared was roughly double the sequential interventions in most transmission settings. Openmalaria simulations of this medical control augmentation of an IRS campaign show an even stronger response with the same timing relationship.

Conclusions

The strong synergies found for these control tools between the complementary interventions demonstrate a general feature of effective concurrent campaign-style vector and medical interventions. A mass treatment campaign is normally short-lived, especially in higher transmission settings. When co-timed, the rapid clearing of the host parasite reservoir via chemotherapy is protected from resurgence by the longer duration of the vector control. An effective synchronous treatment campaign has the potential to greatly augment the impact of indoor residual spraying. Mass screening and treatment (MSAT) with highly sensitive rapid diagnostic tests may demonstrate a comparable trend while mass LLIN campaigns may similarly coordinate with MDA/MSAT.
Appendix
Available only for authorised users
Footnotes
1
The noted exception that an estimated 15–25 million children received seasonal malaria chemoprophylaxis [1, 77].
 
Literature
1.
go back to reference WHO. World malaria report 2017. Geneva: World Health Organization; 2018. WHO. World malaria report 2017. Geneva: World Health Organization; 2018.
2.
go back to reference Breman JG, Egan A, Keusch GT. The intolerable burden of malaria: a new look at the numbers. Am J Trop Med Hyg. 2001;64(1—-2 Suppl):6–8. Breman JG, Egan A, Keusch GT. The intolerable burden of malaria: a new look at the numbers. Am J Trop Med Hyg. 2001;64(1—-2 Suppl):6–8.
3.
go back to reference Malaney PI, Spielman A, Sachs JD. The malaria gap. Am J Trop Med Hyg. 2004;71(2 Suppl):141–6.CrossRef Malaney PI, Spielman A, Sachs JD. The malaria gap. Am J Trop Med Hyg. 2004;71(2 Suppl):141–6.CrossRef
4.
go back to reference Chima RI, Goodman CA, Mills A. The economic impact of malaria in Africa: a critical review of the evidence. Health Policy. 2003;63:17–36.CrossRef Chima RI, Goodman CA, Mills A. The economic impact of malaria in Africa: a critical review of the evidence. Health Policy. 2003;63:17–36.CrossRef
5.
go back to reference Steketee R, Campbell CC. Impact of national malaria control scale-up programmes in Africa: magnitude and attribution of effects. Malar J. 2010;9:299.CrossRef Steketee R, Campbell CC. Impact of national malaria control scale-up programmes in Africa: magnitude and attribution of effects. Malar J. 2010;9:299.CrossRef
6.
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.CrossRef 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.CrossRef
7.
go back to reference Yakob L, Dunning R, Yan G. Searching for synergies in malaria control through integrated vector management. Lancet Infect Dis. 2013;3:112.CrossRef Yakob L, Dunning R, Yan G. Searching for synergies in malaria control through integrated vector management. Lancet Infect Dis. 2013;3:112.CrossRef
8.
go back to reference Fullman N, Burstein R, Lim SS, Medlin C, Gakidou E. Nets, spray or both? The effectiveness of insecticide-treated nets and indoor residual spraying in reducing malaria morbidity and child mortality in sub-Saharan Africa. Malar J. 2013;12:62.CrossRef Fullman N, Burstein R, Lim SS, Medlin C, Gakidou E. Nets, spray or both? The effectiveness of insecticide-treated nets and indoor residual spraying in reducing malaria morbidity and child mortality in sub-Saharan Africa. Malar J. 2013;12:62.CrossRef
9.
go back to reference Protopopoff N, Mosha JF, Lukole E, Charlwood JD, Wright A, Mwalimu CD, et al. Effectiveness of a long-lasting piperonyl butoxide-treated insecticidal net and indoor residual spray interventions, separately and together, against malaria transmitted by pyrethroid-resistant mosquitoes: a cluster, randomised controlled, two-by-two factorial design trial. Lancet. 2018;391:1577–88.CrossRef Protopopoff N, Mosha JF, Lukole E, Charlwood JD, Wright A, Mwalimu CD, et al. Effectiveness of a long-lasting piperonyl butoxide-treated insecticidal net and indoor residual spray interventions, separately and together, against malaria transmitted by pyrethroid-resistant mosquitoes: a cluster, randomised controlled, two-by-two factorial design trial. Lancet. 2018;391:1577–88.CrossRef
10.
go back to reference Farenhorst M, Knols BG, Thomas MB, Howard AF, Takken W, Rowland M, et al. Synergy in efficacy of fungal entomopathogens and permethrin against West African insecticide-resistant Anopheles gambiae mosquitoes. PLoS One. 2010;5:e12081.CrossRef Farenhorst M, Knols BG, Thomas MB, Howard AF, Takken W, Rowland M, et al. Synergy in efficacy of fungal entomopathogens and permethrin against West African insecticide-resistant Anopheles gambiae mosquitoes. PLoS One. 2010;5:e12081.CrossRef
11.
go back to reference Artzy-Randrup Y, Dobson AP, Pascual M. Synergistic and antagonistic interactions between bednets and vaccines in the control of malaria. Proc Nat Acad Sci USA. 2015;112:3014.CrossRef Artzy-Randrup Y, Dobson AP, Pascual M. Synergistic and antagonistic interactions between bednets and vaccines in the control of malaria. Proc Nat Acad Sci USA. 2015;112:3014.CrossRef
12.
go back to reference Gimnig JE, Otieno P, Were V, Marwanga D, Abong’o D, Wiegand R, et al. The effect of indoor residual spraying on the prevalence of malaria parasite infection, clinical malaria and anemia in an area of perennial transmission and moderate coverage of insecticide treated nets in Western Kenya. PLoS One. 2016;11:e0145282.CrossRef Gimnig JE, Otieno P, Were V, Marwanga D, Abong’o D, Wiegand R, et al. The effect of indoor residual spraying on the prevalence of malaria parasite infection, clinical malaria and anemia in an area of perennial transmission and moderate coverage of insecticide treated nets in Western Kenya. PLoS One. 2016;11:e0145282.CrossRef
13.
go back to reference Katureebe A, Zinszer K, Arinaitwe E, Rek J, Kakande E, Charland K, et al. Measures of malaria burden after long-lasting insecticidal net distribution and indoor residual spraying at three sites in Uganda: a prospective observational study. PLoS Med. 2016;13:e1002167.CrossRef Katureebe A, Zinszer K, Arinaitwe E, Rek J, Kakande E, Charland K, et al. Measures of malaria burden after long-lasting insecticidal net distribution and indoor residual spraying at three sites in Uganda: a prospective observational study. PLoS Med. 2016;13:e1002167.CrossRef
14.
go back to reference Rowland M, Boko P, Odjo A, Asidi A, Akogbeto M, N’Guessan R. A new long-lasting indoor residual formulation of the organophosphate insecticide pirimiphos methyl for prolonged control of pyrethroid-resistant mosquitoes: an experimental hut trial in Benin. PLoS One. 2013;8:e69516.CrossRef Rowland M, Boko P, Odjo A, Asidi A, Akogbeto M, N’Guessan R. A new long-lasting indoor residual formulation of the organophosphate insecticide pirimiphos methyl for prolonged control of pyrethroid-resistant mosquitoes: an experimental hut trial in Benin. PLoS One. 2013;8:e69516.CrossRef
15.
go back to reference Gueye CS, Newby G, Gosling RD, Whittaker MA, Chandramohan D, Slutsker L, et al. Strategies and approaches to vector control in nine malaria-eliminating countries: a cross-case study analysis. Malar J. 2016;15:2.CrossRef Gueye CS, Newby G, Gosling RD, Whittaker MA, Chandramohan D, Slutsker L, et al. Strategies and approaches to vector control in nine malaria-eliminating countries: a cross-case study analysis. Malar J. 2016;15:2.CrossRef
16.
go back to reference Oxborough RM. Trends in US President’s Malaria Initiative-funded indoor residual spray coverage and insecticide choice in sub-Saharan Africa (2008–2015): urgent need for affordable, long-lasting insecticides. Malar J. 2016;15:146.CrossRef Oxborough RM. Trends in US President’s Malaria Initiative-funded indoor residual spray coverage and insecticide choice in sub-Saharan Africa (2008–2015): urgent need for affordable, long-lasting insecticides. Malar J. 2016;15:146.CrossRef
17.
go back to reference Okell LC, Drakeley CJ, Ghani AC, Bousema T, Sutherland CJ. Reduction of transmission from malaria patients by artemisinin combination therapies: a pooled analysis of six randomized trials. Malar J. 2008;7:125.CrossRef Okell LC, Drakeley CJ, Ghani AC, Bousema T, Sutherland CJ. Reduction of transmission from malaria patients by artemisinin combination therapies: a pooled analysis of six randomized trials. Malar J. 2008;7:125.CrossRef
18.
go back to reference Barnes KI, Chanda P, ab Barnabas G. Impact of the large-scale deployment of artemether/lumefantrine on the malaria disease burden in Africa: case studies of South Africa, Zambia and Ethiopia. Malar J. 2009;8(Suppl. 1):S8.CrossRef Barnes KI, Chanda P, ab Barnabas G. Impact of the large-scale deployment of artemether/lumefantrine on the malaria disease burden in Africa: case studies of South Africa, Zambia and Ethiopia. Malar J. 2009;8(Suppl. 1):S8.CrossRef
19.
go back to reference Korenromp E, Mahiané G, Hamilton M, Pretorius C, Cibulskis R, Lauer J, et al. Malaria intervention scale-up in Africa: effectiveness predictions for health programme planning tools, based on dynamic transmission modelling. Malar J. 2016;15:417.CrossRef Korenromp E, Mahiané G, Hamilton M, Pretorius C, Cibulskis R, Lauer J, et al. Malaria intervention scale-up in Africa: effectiveness predictions for health programme planning tools, based on dynamic transmission modelling. Malar J. 2016;15:417.CrossRef
20.
go back to reference Elliott RC, Smith DL, Echodu D. Medical and entomological malarial interventions, a comparison and synergy of two control measures using a Ross/Macdonald model variant and openmalaria simulation. Math Biosci. 2018;300:187–200.CrossRef Elliott RC, Smith DL, Echodu D. Medical and entomological malarial interventions, a comparison and synergy of two control measures using a Ross/Macdonald model variant and openmalaria simulation. Math Biosci. 2018;300:187–200.CrossRef
21.
go back to reference Okell LC, Griffin JT, Kleinschmidt I, Hollingsworth TD, Churcher TS, White MJ, et al. The potential contribution of mass treatment to the control of Plasmodium falciparum malaria. PLoS One. 2011;6:e20179.CrossRef Okell LC, Griffin JT, Kleinschmidt I, Hollingsworth TD, Churcher TS, White MJ, et al. The potential contribution of mass treatment to the control of Plasmodium falciparum malaria. PLoS One. 2011;6:e20179.CrossRef
22.
go back to reference Molineaux L, Gramiccia G. The Garki project. Geneva: World Health Organization; 1980. Molineaux L, Gramiccia G. The Garki project. Geneva: World Health Organization; 1980.
24.
go back to reference Liu XZ, Xu BL. Malaria situation and evaluation on the control effect in Henan Province during 1990–2005. Chin J Parasitol Parasit Dis. 2006;24:226. Liu XZ, Xu BL. Malaria situation and evaluation on the control effect in Henan Province during 1990–2005. Chin J Parasitol Parasit Dis. 2006;24:226.
25.
go back to reference Zulueta JD. A malaria eradication experiment in the highlands of Kigezi (Uganda). East Afr Med J. 1964;41:102.PubMed Zulueta JD. A malaria eradication experiment in the highlands of Kigezi (Uganda). East Afr Med J. 1964;41:102.PubMed
26.
go back to reference Kaneko A, Taleo G, Kalkoa M, Yamar S, Kobayakawa T, Bjorkman A. Malaria eradication on islands. Lancet. 2000;356:1560–4.CrossRef Kaneko A, Taleo G, Kalkoa M, Yamar S, Kobayakawa T, Bjorkman A. Malaria eradication on islands. Lancet. 2000;356:1560–4.CrossRef
27.
go back to reference Newby G, Hwang J, Koita K, Chen I, Greenwood B, von Seidlein L, et al. Review of mass drug administration for malaria and its operational challenges. Am J Trop Med Hyg. 2015;93:125–34.CrossRef Newby G, Hwang J, Koita K, Chen I, Greenwood B, von Seidlein L, et al. Review of mass drug administration for malaria and its operational challenges. Am J Trop Med Hyg. 2015;93:125–34.CrossRef
28.
go back to reference Poirot E, Skarbinski J, Sinclair D, Kachur SP, Slutsker L, Hwang J. Mass drug administration for malaria. Cochrane Database Syst Rev. 2013;12:CD008846. Poirot E, Skarbinski J, Sinclair D, Kachur SP, Slutsker L, Hwang J. Mass drug administration for malaria. Cochrane Database Syst Rev. 2013;12:CD008846.
29.
go back to reference Eisele TP, Silumbe K, Finn T, Chalwe V, Kamuliwo M, Hamainza B, et al. Assessing the effectiveness of household-level focal mass drug administration and community-wide mass drug administration for reducing malaria parasite infection prevalence and incidence in Southern Province, Zambia: study protocol for a community randomized controlled trial. Trials. 2015;16:347.CrossRef Eisele TP, Silumbe K, Finn T, Chalwe V, Kamuliwo M, Hamainza B, et al. Assessing the effectiveness of household-level focal mass drug administration and community-wide mass drug administration for reducing malaria parasite infection prevalence and incidence in Southern Province, Zambia: study protocol for a community randomized controlled trial. Trials. 2015;16:347.CrossRef
30.
go back to reference Sharp BL, Ridl FC, Govender D, Kuklinski J, Kleinschmidt I. Malaria vector control by indoor residual insecticide spraying on the tropical island of Bioko, Equatorial Guinea. Malar J. 2007;6:52.CrossRef Sharp BL, Ridl FC, Govender D, Kuklinski J, Kleinschmidt I. Malaria vector control by indoor residual insecticide spraying on the tropical island of Bioko, Equatorial Guinea. Malar J. 2007;6:52.CrossRef
31.
go back to reference Pluess B, Tanser FC, Lengeler C, Sharp BL. Indoor residual spraying for preventing malaria. Cochrane Database Syst Rev. 2010;4:CD006657. Pluess B, Tanser FC, Lengeler C, Sharp BL. Indoor residual spraying for preventing malaria. Cochrane Database Syst Rev. 2010;4:CD006657.
32.
go back to reference Wen S, Harvard KE, Gueye CS, Canavati SE, Chancellor A, et al. Targeting populations at higher risk for malaria: a survey of national malaria elimination programmes in the Asia Pacific. Malar J. 2016;15:271.CrossRef Wen S, Harvard KE, Gueye CS, Canavati SE, Chancellor A, et al. Targeting populations at higher risk for malaria: a survey of national malaria elimination programmes in the Asia Pacific. Malar J. 2016;15:271.CrossRef
33.
go back to reference O’Meara WP, Mangeni JN, Steketee R, Greenwood B. Changes in the burden of malaria in sub-Saharan Africa. Lancet Infect Dis. 2010;10:545–55.CrossRef O’Meara WP, Mangeni JN, Steketee R, Greenwood B. Changes in the burden of malaria in sub-Saharan Africa. Lancet Infect Dis. 2010;10:545–55.CrossRef
34.
go back to reference Bhatt S, Weiss DJ, Cameron E, Bisanzio D, Mappio B, Dalrymple U, et al. The effect of malaria control on Plasmodium falciparum in Africa between 2000 and 2015. Nature. 2015;526:207–11.CrossRef Bhatt S, Weiss DJ, Cameron E, Bisanzio D, Mappio B, Dalrymple U, et al. The effect of malaria control on Plasmodium falciparum in Africa between 2000 and 2015. Nature. 2015;526:207–11.CrossRef
35.
go back to reference Eisele TP, Bennett A, Silumbe K, Finn TP, Chalwe V, Kamuliwo M, et al. Short-term impact of mass drug administration with dihydroartemisinin plus piperaquine on malaria in Southern Province Zambia: a cluster-randomized controlled trial. J Infect Dis. 2016;214:1831–9.CrossRef Eisele TP, Bennett A, Silumbe K, Finn TP, Chalwe V, Kamuliwo M, et al. Short-term impact of mass drug administration with dihydroartemisinin plus piperaquine on malaria in Southern Province Zambia: a cluster-randomized controlled trial. J Infect Dis. 2016;214:1831–9.CrossRef
36.
go back to reference Organization WH. Mass drug administration, mass screening and treatment and focal screening and treatment for malaria. Geneva: World Health Organization; 2015a. Organization WH. Mass drug administration, mass screening and treatment and focal screening and treatment for malaria. Geneva: World Health Organization; 2015a.
37.
go back to reference McCord GC, Anttila-Hughes JK. A malaria ecology index predicted spatial and temporal variation of malaria burden and efficacy of antimalarial interventions based on African serological data. Am J Trop Med Hyg. 2017;96:616.PubMedPubMedCentral McCord GC, Anttila-Hughes JK. A malaria ecology index predicted spatial and temporal variation of malaria burden and efficacy of antimalarial interventions based on African serological data. Am J Trop Med Hyg. 2017;96:616.PubMedPubMedCentral
38.
go back to reference Kigozi R, Baxi SM, Gasasira A, Sserwanga A, Kakeeto S, Nasr S, et al. Indoor residual spraying of insecticide and malaria morbidity in a high transmission intensity area of Uganda. PLoS ONE. 2012;7:e42857.CrossRef Kigozi R, Baxi SM, Gasasira A, Sserwanga A, Kakeeto S, Nasr S, et al. Indoor residual spraying of insecticide and malaria morbidity in a high transmission intensity area of Uganda. PLoS ONE. 2012;7:e42857.CrossRef
39.
go back to reference Macdonald G. Epidemiological basis of malaria control. Bull World Health Org. 1956;15:613.PubMed Macdonald G. Epidemiological basis of malaria control. Bull World Health Org. 1956;15:613.PubMed
40.
go back to reference Stuckey EM, Stevenson JC, Galactionova K, Baidjoe AY, Bousema T, Odongo W, et al. Modeling the cost effectiveness of malaria control interventions in the highlands of western Kenya. PLoS ONE. 2014;9:e107700.CrossRef Stuckey EM, Stevenson JC, Galactionova K, Baidjoe AY, Bousema T, Odongo W, et al. Modeling the cost effectiveness of malaria control interventions in the highlands of western Kenya. PLoS ONE. 2014;9:e107700.CrossRef
41.
go back to reference Okell L, Slater H, Ghani A, Pemberton-Ross P, Smith TA, Chitnis N. Consensus modelling evidence to support the design of mass drug administration programmes. In: Background document for session I. Malaria policy advisory committee meeting, 16–18 Sept. 2015. Geneva: World Health Organization; 2015. Okell L, Slater H, Ghani A, Pemberton-Ross P, Smith TA, Chitnis N. Consensus modelling evidence to support the design of mass drug administration programmes. In: Background document for session I. Malaria policy advisory committee meeting, 16–18 Sept. 2015. Geneva: World Health Organization; 2015.
42.
go back to reference Chitnis N, Schapira A, Smith T, Steketee R. Comparing the effectiveness of malaria vector–control interventions through a mathematical model. Am J Trop Med Hyg. 2010;83:230.CrossRef Chitnis N, Schapira A, Smith T, Steketee R. Comparing the effectiveness of malaria vector–control interventions through a mathematical model. Am J Trop Med Hyg. 2010;83:230.CrossRef
43.
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:e1000324.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:e1000324.CrossRef
44.
go back to reference Griffin JT. The interaction between seasonality and pulsed interventions against malaria in their effects on the reproduction number. PLoS Comp Biol. 2015;11:e1004057.CrossRef Griffin JT. The interaction between seasonality and pulsed interventions against malaria in their effects on the reproduction number. PLoS Comp Biol. 2015;11:e1004057.CrossRef
45.
go back to reference White MT, Griffin JT, Churcher TS, Ferguson NM, Basanez MG, Ghani AC. Modelling the impact of vector control interventions on Anopheles gambiae population dynamics. Parasit Vectors. 2011;4:153.CrossRef White MT, Griffin JT, Churcher TS, Ferguson NM, Basanez MG, Ghani AC. Modelling the impact of vector control interventions on Anopheles gambiae population dynamics. Parasit Vectors. 2011;4:153.CrossRef
46.
go back to reference Smith DL, McKenzie FE. Statics and dynamics of malaria infection in Anopheles mosquitoes. Malar J. 2004;3:13.CrossRef Smith DL, McKenzie FE. Statics and dynamics of malaria infection in Anopheles mosquitoes. Malar J. 2004;3:13.CrossRef
47.
go back to reference Bekessy A, Molineaux L, Storey J. Estimation of incidence and recovery rates of Plasmodium falciparum parasitaemia from longitudinal data. Bull World Health Org. 1976;54:685–93.PubMed Bekessy A, Molineaux L, Storey J. Estimation of incidence and recovery rates of Plasmodium falciparum parasitaemia from longitudinal data. Bull World Health Org. 1976;54:685–93.PubMed
48.
go back to reference Smith DL, Hay SI, Noor AM, Snow RW. Predicting changing malaria risk after expanded insecticide-treated net coverage in Africa. Trends Parasitol. 2009;25:511.CrossRef Smith DL, Hay SI, Noor AM, Snow RW. Predicting changing malaria risk after expanded insecticide-treated net coverage in Africa. Trends Parasitol. 2009;25:511.CrossRef
49.
go back to reference Smith T, Schapira A. Reproduction numbers in malaria and their implications. Trends Parasitol. 2012;28:3–8.CrossRef Smith T, Schapira A. Reproduction numbers in malaria and their implications. Trends Parasitol. 2012;28:3–8.CrossRef
50.
go back to reference Anderson RM, May RM. Infectious diseases of humans: dynamics and control. Oxford: Oxford University Press; 1992. Anderson RM, May RM. Infectious diseases of humans: dynamics and control. Oxford: Oxford University Press; 1992.
51.
go back to reference Barthélemy M, Barrat A, Pastor-Satorras R, Vespignani A. Velocity and hierarchical spread of epidemic outbreaks in scale-free networks. Phys Rev Lett. 2004;92:178701.CrossRef Barthélemy M, Barrat A, Pastor-Satorras R, Vespignani A. Velocity and hierarchical spread of epidemic outbreaks in scale-free networks. Phys Rev Lett. 2004;92:178701.CrossRef
52.
go back to reference Smith DL, Battle KE, Hay SI, Barker CM, Scott TW, McKenzie FE. Ross, Macdonald, and a theory for the dynamics and control of mosquito-transmitted pathogens. PLoS Pathog. 2012;8:e1002588.CrossRef Smith DL, Battle KE, Hay SI, Barker CM, Scott TW, McKenzie FE. Ross, Macdonald, and a theory for the dynamics and control of mosquito-transmitted pathogens. PLoS Pathog. 2012;8:e1002588.CrossRef
53.
go back to reference Smith T, Killeen GF, Maire N, Ross A, Molineaux L, Tediosi F, et al. Mathematical modeling of the impact of malaria vaccines on the clinical epidemiology and natural history of Plasmodium falciparum malaria: overview. Am J Trop Med Hyg. 2006;75(2 Suppl):1–10.CrossRef Smith T, Killeen GF, Maire N, Ross A, Molineaux L, Tediosi F, et al. Mathematical modeling of the impact of malaria vaccines on the clinical epidemiology and natural history of Plasmodium falciparum malaria: overview. Am J Trop Med Hyg. 2006;75(2 Suppl):1–10.CrossRef
54.
go back to reference Maire N, Smith T, Ross A, Owusu-Agyei S, Dietz K, Molineaux L. A model for natural immunity to asexual blood stages of Plasmodium falciparum malaria in endemic areas. Am J Trop Med Hyg. 2006;75(2–suppl):19–31.CrossRef Maire N, Smith T, Ross A, Owusu-Agyei S, Dietz K, Molineaux L. A model for natural immunity to asexual blood stages of Plasmodium falciparum malaria in endemic areas. Am J Trop Med Hyg. 2006;75(2–suppl):19–31.CrossRef
55.
go back to reference Ross A, Maire N, Molineaux L, Smith T. An epidemiologic model of severe morbidity and mortality caused by Plasmodium falciparum. Am J Trop Med Hyg. 2006;75(2–suppl):63–73.CrossRef Ross A, Maire N, Molineaux L, Smith T. An epidemiologic model of severe morbidity and mortality caused by Plasmodium falciparum. Am J Trop Med Hyg. 2006;75(2–suppl):63–73.CrossRef
56.
go back to reference Smith T, Ross A, Maire N, Rogier C, Trape JF, Molineaux L. An epidemiologic model of the incidence of acute illness in Plasmodium falciparum malaria. Am J Trop Med Hyg. 2006;75(2–suppl):56–62.CrossRef Smith T, Ross A, Maire N, Rogier C, Trape JF, Molineaux L. An epidemiologic model of the incidence of acute illness in Plasmodium falciparum malaria. Am J Trop Med Hyg. 2006;75(2–suppl):56–62.CrossRef
57.
go back to reference Smith T, Maire N, Dietz K, Killeen GF, Vounatsou P, Molineaux L, et al. Relationship between the entomologic inoculation rate and the force of infection for Plasmodium falciparum malaria. Am J Trop Med Hyg. 2006;75(2–suppl):11–8.CrossRef Smith T, Maire N, Dietz K, Killeen GF, Vounatsou P, Molineaux L, et al. Relationship between the entomologic inoculation rate and the force of infection for Plasmodium falciparum malaria. Am J Trop Med Hyg. 2006;75(2–suppl):11–8.CrossRef
58.
go back to reference Ross A, Killeen G, Smith T. Relationships between host infectivity to mosquitoes and asexual parasite density in Plasmodium falciparum. Am J Trop Med Hyg. 2006;75(2–suppl):32–7.CrossRef Ross A, Killeen G, Smith T. Relationships between host infectivity to mosquitoes and asexual parasite density in Plasmodium falciparum. Am J Trop Med Hyg. 2006;75(2–suppl):32–7.CrossRef
59.
go back to reference Galactinova K, Tediosi F, de Savigny D, Smith T, Tanner M. Effective coverage and systems effectiveness for malaria case management in sub-Saharan African countries. PLoS Med. 2012;10:e0127818.CrossRef Galactinova K, Tediosi F, de Savigny D, Smith T, Tanner M. Effective coverage and systems effectiveness for malaria case management in sub-Saharan African countries. PLoS Med. 2012;10:e0127818.CrossRef
60.
go back to reference Smith T, Ross A, Maire N, Chitnis N, Studer A, Hardy D, et al. Ensemble modeling of the likely public health impact of a pre-erythrocytic malaria vaccine. PLoS Med. 2012;9:e1001157.CrossRef Smith T, Ross A, Maire N, Chitnis N, Studer A, Hardy D, et al. Ensemble modeling of the likely public health impact of a pre-erythrocytic malaria vaccine. PLoS Med. 2012;9:e1001157.CrossRef
61.
go back to reference Griffin JT. Is a reproduction number of one a threshold for Plasmodium falciparum malaria elimination? Malar J. 2016;15:389.CrossRef Griffin JT. Is a reproduction number of one a threshold for Plasmodium falciparum malaria elimination? Malar J. 2016;15:389.CrossRef
62.
go back to reference Menach AL, McKenzie FE, Flahault A, Smith DL. The unexpected importance of mosquito oviposition behaviour for malaria: non-productive larval habitats can be sources for malaria transmission. Malar J. 2005;4:23.CrossRef Menach AL, McKenzie FE, Flahault A, Smith DL. The unexpected importance of mosquito oviposition behaviour for malaria: non-productive larval habitats can be sources for malaria transmission. Malar J. 2005;4:23.CrossRef
63.
go back to reference Killeen GF, Knols BGJ, Gu W. Taking malaria transmission out of the bottle: implications of mosquito dispersal for vector-control interventions. Lancet. 2003;3:297–303.CrossRef Killeen GF, Knols BGJ, Gu W. Taking malaria transmission out of the bottle: implications of mosquito dispersal for vector-control interventions. Lancet. 2003;3:297–303.CrossRef
64.
go back to reference Smith DL, Dushoff J, McKenzie FE. The risk of a mosquito-borne infection in a heterogeneous environment. PLoS Biol. 2004;2:e368.CrossRef Smith DL, Dushoff J, McKenzie FE. The risk of a mosquito-borne infection in a heterogeneous environment. PLoS Biol. 2004;2:e368.CrossRef
65.
go back to reference Prosper O, Ruktanonchai NW, Martcheva M. Assessing the role of spatial heterogeneity and human movement in malaria dynamics and control. J Theor Biol. 2012;303:1–14.CrossRef Prosper O, Ruktanonchai NW, Martcheva M. Assessing the role of spatial heterogeneity and human movement in malaria dynamics and control. J Theor Biol. 2012;303:1–14.CrossRef
66.
go back to reference Ruktanonchai NW, DeLeenheer P, Tatum AJ, Alegana VA, Caughlin TT, zu Erbach-Schoenberg E, et al. Identifying malaria transmission foci for elimination using human mobility data. PLoS Comput Biol. 2012;12:e1004846.CrossRef Ruktanonchai NW, DeLeenheer P, Tatum AJ, Alegana VA, Caughlin TT, zu Erbach-Schoenberg E, et al. Identifying malaria transmission foci for elimination using human mobility data. PLoS Comput Biol. 2012;12:e1004846.CrossRef
67.
go back to reference Prothero RM. Disease and mobility: a neglected factor in epidemiology. Int J Epidemiol. 1977;6:259–67.CrossRef Prothero RM. Disease and mobility: a neglected factor in epidemiology. Int J Epidemiol. 1977;6:259–67.CrossRef
68.
go back to reference Dietz K, Molineaux L, Thomas A. A malaria model tested in the African Savannah. Bull World Health Org. 1974;50:347–57.PubMed Dietz K, Molineaux L, Thomas A. A malaria model tested in the African Savannah. Bull World Health Org. 1974;50:347–57.PubMed
69.
go back to reference Reiner RC, Perkins TA, Barker CM, Niu T, Chaves LF, et al. A systematic review of mathematical models of mosquito-borne pathogen transmission: 1970–2010. J R Soc Interface. 2013;10:20120921.CrossRef Reiner RC, Perkins TA, Barker CM, Niu T, Chaves LF, et al. A systematic review of mathematical models of mosquito-borne pathogen transmission: 1970–2010. J R Soc Interface. 2013;10:20120921.CrossRef
70.
go back to reference Ross R. The prevention of malaria. London: John Murray; 1911. Ross R. The prevention of malaria. London: John Murray; 1911.
71.
go back to reference Bonnet S, Gouagna C, Safeukui I, Meunier JY, Boudin C. Comparison of artificial membrane feeding with direct skin feeding to estimate infectiousness of Plasmodium falciparum gametocyte carriers to mosquitoes. Trans R Soc Trop Med Hyg. 2000;94:103–6.CrossRef Bonnet S, Gouagna C, Safeukui I, Meunier JY, Boudin C. Comparison of artificial membrane feeding with direct skin feeding to estimate infectiousness of Plasmodium falciparum gametocyte carriers to mosquitoes. Trans R Soc Trop Med Hyg. 2000;94:103–6.CrossRef
73.
go back to reference Chitnis N, Smith T, Steketee R. A mathematical model for the dynamics of malaria in mosquitoes feeding on a heterogeneous host population. J Biol Dyn. 2008;2:259–85.CrossRef Chitnis N, Smith T, Steketee R. A mathematical model for the dynamics of malaria in mosquitoes feeding on a heterogeneous host population. J Biol Dyn. 2008;2:259–85.CrossRef
74.
go back to reference Chitnis N, Hardy D, Smith T. A periodically-forced mathematical model for the seasonal dynamics of malaria in mosquitoes. Bull Math Biol. 2012;74:1098–124.CrossRef Chitnis N, Hardy D, Smith T. A periodically-forced mathematical model for the seasonal dynamics of malaria in mosquitoes. Bull Math Biol. 2012;74:1098–124.CrossRef
75.
go back to reference Stuckey EM, Stevenson JC, Cooke MK, Owaga C, Marube E, Oando G, et al. Simulation of malaria epidemiology and control in the highlands of western Kenya. Malar J. 2012;11:357.CrossRef Stuckey EM, Stevenson JC, Cooke MK, Owaga C, Marube E, Oando G, et al. Simulation of malaria epidemiology and control in the highlands of western Kenya. Malar J. 2012;11:357.CrossRef
77.
go back to reference Cisse B, Sokhna C, NDiaye JL, Pitt JFGYDC, NDiaye M, Cairns M, et al. Effectiveness of seasonal malaria chemoprevention in children under ten years of age in Senegal: a stepped-wedge cluster-randomised trial. PLoS Med. 2016;13:e1002175.CrossRef Cisse B, Sokhna C, NDiaye JL, Pitt JFGYDC, NDiaye M, Cairns M, et al. Effectiveness of seasonal malaria chemoprevention in children under ten years of age in Senegal: a stepped-wedge cluster-randomised trial. PLoS Med. 2016;13:e1002175.CrossRef
78.
go back to reference Press WH, Teukolsky SA, Vetterling WT, Flannery BP. Numerical recipes in C++. The art of scientific computing. 1992. Press WH, Teukolsky SA, Vetterling WT, Flannery BP. Numerical recipes in C++. The art of scientific computing. 1992.
Metadata
Title
Synergy and timing: a concurrent mass medical campaign predicted to augment indoor residual spraying for malaria
Authors
Richard C. Elliott
David L. Smith
Dorothy C. Echodu
Publication date
01-12-2019
Publisher
BioMed Central
Keyword
Malaria
Published in
Malaria Journal / Issue 1/2019
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-019-2788-9

Other articles of this Issue 1/2019

Malaria Journal 1/2019 Go to the issue
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discuss last year's major advances in heart failure and cardiomyopathies.