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Published in: Malaria Journal 1/2017

Open Access 01-12-2017 | Research

Modelling the impact of the long-term use of insecticide-treated bed nets on Anopheles mosquito biting time

Authors: Claudia P. Ferreira, Silas P. Lyra, Franciane Azevedo, David Greenhalgh, Eduardo Massad

Published in: Malaria Journal | Issue 1/2017

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Abstract

Background

Evidence of changing in biting and resting behaviour of the main malaria vectors has been mounting up in recent years as a result of selective pressure by the widespread and long-term use of insecticide-treated bed nets (ITNs), and indoor residual spraying. The impact of resistance behaviour on malaria intervention efficacy has important implications for the epidemiology and malaria control programmes. In this context, a theoretical framework is presented to understand the mechanisms determining the evolution of feeding behaviour under the pressure of use of ITNs.

Methods

An agent-based stochastic model simulates the impact of insecticide-treated bed nets on mosquito fitness by reducing the biting rates, as well as increasing mortality rates. The model also incorporates a heritability function that provides the necessary genetic plasticity upon which natural selection would act to maximize the fitness under the pressure of the control strategy.

Results

The asymptotic equilibrium distribution of mosquito population versus biting time is shown for several daily uses of ITNs, and the expected disruptive selection on this mosquito trait is observed in the simulations. The relative fitness of strains that bite at much earlier time with respect to the wild strains, when a threshold of about 50% of ITNs coverage highlights the hypothesis of a behaviour selection. A sensitivity analysis has shown that the top three parameters that play a dominant role on the mosquito fitness are the proportion of individuals using bed nets and its effectiveness, the impact of bed nets on mosquito oviposition, and the mosquito genetic plasticity related to changing in biting time.

Conclusion

By taking the evolutionary aspect into account, the model was able to show that the long-term use of ITNs, although representing an undisputed success in reducing malaria incidence and mortality in many affected areas, is not free of undesirable side effects. From the evolutionary point of view of the parasite virulence, it should be expected that plasmodium parasites would be under pressure to reduce their virulence. This speculative hypothesis can eventually be demonstrated in the medium to long-term use of ITNs.
Literature
1.
go back to reference Phillips-Howard PA, Nahlen BL, Kolczak MS, Hightower AW, ter Kuile FO, Alaii JA, et al. Efficacy of permethrin-treated bed nets in the prevention of mortality in young children in an area of high perennial malaria transmission in western Kenya. Am J Trop Med Hyg. 2003;68:23–9.PubMed Phillips-Howard PA, Nahlen BL, Kolczak MS, Hightower AW, ter Kuile FO, Alaii JA, et al. Efficacy of permethrin-treated bed nets in the prevention of mortality in young children in an area of high perennial malaria transmission in western Kenya. Am J Trop Med Hyg. 2003;68:23–9.PubMed
4.
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;15:225.CrossRefPubMedPubMedCentral 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;15:225.CrossRefPubMedPubMedCentral
5.
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;15:76.CrossRefPubMedPubMedCentral 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;15:76.CrossRefPubMedPubMedCentral
6.
9.
go back to reference Russel 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 predominantly outdoors. Malar J. 2016;15:156.CrossRef Russel 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 predominantly outdoors. Malar J. 2016;15:156.CrossRef
10.
go back to reference Russel TL, Beebe NW, Bugoro H, Apairamo A, Cooper RD, Collins FH, et al. Determinants of host feeding success by \(Anopheles\, farauti\). Malar J. 2016;15:152.CrossRef Russel TL, Beebe NW, Bugoro H, Apairamo A, Cooper RD, Collins FH, et al. Determinants of host feeding success by \(Anopheles\, farauti\). Malar J. 2016;15:152.CrossRef
11.
12.
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;25:511–6.CrossRefPubMedPubMedCentral Smith DL, Hay SI, Noor AM, Snow RW. Predicting changing malaria risk after expanded insecticide-treated net coverage in Africa. Trends Parasitol. 2009;25:511–6.CrossRefPubMedPubMedCentral
13.
go back to reference Sougoufara S, Diédhiou SM, Doucouré S, Diagne N, Sembéne 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, Sembéne 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
14.
go back to reference Velema JP, Alihonou EM, Gandaho T, Hounye FH. Childhood mortality among users and non-users of primary health care in a rural west African community. Int J Epidemiol. 1991;20:474–9.CrossRefPubMed Velema JP, Alihonou EM, Gandaho T, Hounye FH. Childhood mortality among users and non-users of primary health care in a rural west African community. Int J Epidemiol. 1991;20:474–9.CrossRefPubMed
15.
go back to reference Mtango FD, Neuvians D. Acute respiratory infections in children under 5 years. Control project in Bagamoyo District, Tanzania. Trans R Soc Trop Med Hyg. 1986;80:851–8.CrossRefPubMed Mtango FD, Neuvians D. Acute respiratory infections in children under 5 years. Control project in Bagamoyo District, Tanzania. Trans R Soc Trop Med Hyg. 1986;80:851–8.CrossRefPubMed
16.
go back to reference Ototo EN, Mbugi JP, Wanjala CL, Zhou G, Githeko AK, Yan G. Surveillance of malaria vector population density and biting behaviour in western Kenya. Malar J. 2015;14:244.CrossRefPubMedPubMedCentral Ototo EN, Mbugi JP, Wanjala CL, Zhou G, Githeko AK, Yan G. Surveillance of malaria vector population density and biting behaviour in western Kenya. Malar J. 2015;14:244.CrossRefPubMedPubMedCentral
17.
go back to reference Wamae PM, Githeko AK, Otieno GO, Kabiru EW, Duombia SO. Early biting of the \(Anopheles\, gambiae\) s.s. and its challenges to vector control using insecticide treated nets in western Kenya highlands. Acta Trop. 2015;150:136–42.CrossRefPubMed Wamae PM, Githeko AK, Otieno GO, Kabiru EW, Duombia SO. Early biting of the \(Anopheles\, gambiae\) s.s. and its challenges to vector control using insecticide treated nets in western Kenya highlands. Acta Trop. 2015;150:136–42.CrossRefPubMed
18.
go back to reference Lindblade KA, Eisele TP, Gimnig JE, Alaii JA, Odhiambo F, ter Kuile FO, et al. Sustainability of reductions in malaria transmission and infant mortality in western Kenya with use of insecticide-treated bednets: 4 to 6 years of follow-up. JAMA. 2004;291:2571–80.CrossRefPubMed Lindblade KA, Eisele TP, Gimnig JE, Alaii JA, Odhiambo F, ter Kuile FO, et al. Sustainability of reductions in malaria transmission and infant mortality in western Kenya with use of insecticide-treated bednets: 4 to 6 years of follow-up. JAMA. 2004;291:2571–80.CrossRefPubMed
19.
go back to reference Bradley J, Lines J, Fuseini G, Schwabe C, Monti F, Slotman M, et al. Outdoor biting by \(Anopheles\, mosquitoes\) on Bioko Island does not currently impact on malaria control. Malar J. 2015;14:170.CrossRefPubMedPubMedCentral Bradley J, Lines J, Fuseini G, Schwabe C, Monti F, Slotman M, et al. Outdoor biting by \(Anopheles\, mosquitoes\) on Bioko Island does not currently impact on malaria control. Malar J. 2015;14:170.CrossRefPubMedPubMedCentral
20.
go back to reference Ojuka P, Boum-II Y, Denoeud-Ndam L, Nabasumba C, Muller Y, Okia M, et al. Early biting and insecticide resistance in the malaria vector Anopheles might compromise the effectiveness of vector control intervention in Southwestern Uganda. Malar J. 2015;14:148.CrossRefPubMedPubMedCentral Ojuka P, Boum-II Y, Denoeud-Ndam L, Nabasumba C, Muller Y, Okia M, et al. Early biting and insecticide resistance in the malaria vector Anopheles might compromise the effectiveness of vector control intervention in Southwestern Uganda. Malar J. 2015;14:148.CrossRefPubMedPubMedCentral
21.
go back to reference Alonso PL, Lindsay SW, Armstrong JR, Conteh M, Hill AG, David PH, et al. The effect of insecticide-treated bed nets on mortality of Gambian children. Lancet. 1991;337:1499–502.CrossRefPubMed Alonso PL, Lindsay SW, Armstrong JR, Conteh M, Hill AG, David PH, et al. The effect of insecticide-treated bed nets on mortality of Gambian children. Lancet. 1991;337:1499–502.CrossRefPubMed
22.
go back to reference Paintain LS, Awini E, Addei S, Kukula V, Nikoi C, Sarpong D, et al. Evaluation of a universal long-lasting insecticidal net (LLIN) distribution campaign in Ghana: cost effectiveness of distribution and hang-up activities. Malar J. 2014;13:71.CrossRef Paintain LS, Awini E, Addei S, Kukula V, Nikoi C, Sarpong D, et al. Evaluation of a universal long-lasting insecticidal net (LLIN) distribution campaign in Ghana: cost effectiveness of distribution and hang-up activities. Malar J. 2014;13:71.CrossRef
23.
go back to reference Kateera F, Ingabire CM, Hakizimana E, Rulisa A, Karinda P, Grobusch MP, et al. Long-lasting insecticidal net source, ownership and use in the context of universal coverage: a household survey in eastern Rwanda. Malar J. 2015;14:390.CrossRefPubMedPubMedCentral Kateera F, Ingabire CM, Hakizimana E, Rulisa A, Karinda P, Grobusch MP, et al. Long-lasting insecticidal net source, ownership and use in the context of universal coverage: a household survey in eastern Rwanda. Malar J. 2015;14:390.CrossRefPubMedPubMedCentral
25.
go back to reference Lines JD, Myamba J, Curtis CF. Experimental hut trials of permethrin-impregnated mosquito nets and eave curtains against malaria vectors in Tanzania. Med Vet Entomol. 1987;1:37–51.CrossRefPubMed Lines JD, Myamba J, Curtis CF. Experimental hut trials of permethrin-impregnated mosquito nets and eave curtains against malaria vectors in Tanzania. Med Vet Entomol. 1987;1:37–51.CrossRefPubMed
26.
go back to reference Voorham J. Intra-population plasticity of Anopheles darlingi’s (Diptera, Culicidae) biting activity patterns in the state of Amapá, Brazil. Rev Saúde Públ. 2002;36:75–80.CrossRef Voorham J. Intra-population plasticity of Anopheles darlingi’s (Diptera, Culicidae) biting activity patterns in the state of Amapá, Brazil. Rev Saúde Públ. 2002;36:75–80.CrossRef
27.
go back to reference Huho B, Briet O, Seyoum A, Sikaala C, Bayoh N, Gimnig J, et al. Consistently high estimates for the proportion of human exposure to malaria vector populations occurring indoors in rural Africa. Int J Epidemiol. 2013;42:235–47.CrossRefPubMedPubMedCentral Huho B, Briet O, Seyoum A, Sikaala C, Bayoh N, Gimnig J, et al. Consistently high estimates for the proportion of human exposure to malaria vector populations occurring indoors in rural Africa. Int J Epidemiol. 2013;42:235–47.CrossRefPubMedPubMedCentral
28.
go back to reference Russel 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.CrossRef Russel 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.CrossRef
29.
go back to reference Saltelli A, Ratto M, Tarantola S, Campolongo F. Sensitivity analysis for chemical models. Chem Rev. 2005;105:2811–28.CrossRefPubMed Saltelli A, Ratto M, Tarantola S, Campolongo F. Sensitivity analysis for chemical models. Chem Rev. 2005;105:2811–28.CrossRefPubMed
30.
go back to reference Marino S, Hogue IB, Ray CJ, Kirschner DE. A methodology for performing global uncertainty and sensitivity analysis in systems biology. J Theor Biol. 2008;254:178–96.CrossRefPubMedPubMedCentral Marino S, Hogue IB, Ray CJ, Kirschner DE. A methodology for performing global uncertainty and sensitivity analysis in systems biology. J Theor Biol. 2008;254:178–96.CrossRefPubMedPubMedCentral
31.
go back to reference Pates H, Curtis C. Mosquito behavior and vector control. Ann Rev Entomol. 2005;50:53–70.CrossRef Pates H, Curtis C. Mosquito behavior and vector control. Ann Rev Entomol. 2005;50:53–70.CrossRef
32.
go back to reference Briet OJT. A simple method for calculating mosquito mortality rates, correcting for seasonal variations in recruitment. Med Vet Entomol. 2002;16:22–7.CrossRefPubMed Briet OJT. A simple method for calculating mosquito mortality rates, correcting for seasonal variations in recruitment. Med Vet Entomol. 2002;16:22–7.CrossRefPubMed
33.
go back to reference Ewald PW. Evolution of infectious diseases. Oxford: Oxford University Press; 1994. p. 293. Ewald PW. Evolution of infectious diseases. Oxford: Oxford University Press; 1994. p. 293.
34.
go back to reference da Silva DR, Lopez LF, Struchiner CJ, Massad E. A mathematical model to assess the impact of temperature on the virulence of vector-borne pathogens. Appli Math Sci. 2014;8:5065–77. da Silva DR, Lopez LF, Struchiner CJ, Massad E. A mathematical model to assess the impact of temperature on the virulence of vector-borne pathogens. Appli Math Sci. 2014;8:5065–77.
35.
go back to reference Ochomo EO, Bayoh NM, Walker ED, Abongo BO, Ombok MO, Ouma C, et al. The efficacy of long-lasting nets with declining physical integrity may be compromised in areas with high levels of pyrethroid resistance. Malar J. 2013;12:368.CrossRefPubMedPubMedCentral Ochomo EO, Bayoh NM, Walker ED, Abongo BO, Ombok MO, Ouma C, et al. The efficacy of long-lasting nets with declining physical integrity may be compromised in areas with high levels of pyrethroid resistance. Malar J. 2013;12:368.CrossRefPubMedPubMedCentral
Metadata
Title
Modelling the impact of the long-term use of insecticide-treated bed nets on Anopheles mosquito biting time
Authors
Claudia P. Ferreira
Silas P. Lyra
Franciane Azevedo
David Greenhalgh
Eduardo Massad
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/s12936-017-2014-6

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