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Published in: Malaria Journal 1/2019

Open Access 01-12-2019 | Plasmodium Falciparum | Research

Models of effectiveness of interventions against malaria transmitted by Anopheles albimanus

Authors: Olivier J. T. Briët, Daniel E. Impoinvil, Nakul Chitnis, Emilie Pothin, Jean Frantz Lemoine, Joseph Frederic, Thomas A. Smith

Published in: Malaria Journal | Issue 1/2019

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Abstract

Background

Most impact prediction of malaria vector control interventions has been based on African vectors. Anopheles albimanus, the main vector in Central America and the Caribbean, has higher intrinsic mortality, is more zoophilic and less likely to rest indoors. Therefore, relative impact among interventions may be different. Prioritizing interventions, in particular for eliminating Plasmodium falciparum from Haiti, should consider local vector characteristics.

Methods

Field bionomics data of An. albimanus from Hispaniola and intervention effect data from southern Mexico were used to parameterize mathematical malaria models. Indoor residual spraying (IRS), insecticide-treated nets (ITNs), and house-screening were analysed by inferring their impact on the vectorial capacity in a difference-equation model. Impact of larval source management (LSM) was assumed linear with coverage. Case management, mass drug administration and vaccination were evaluated by estimating their effects on transmission in a susceptible-infected-susceptible model. Analogous analyses were done for Anopheles gambiae parameterized with data from Tanzania, Benin and Nigeria.

Results

While LSM was equally effective against both vectors, impact of ITNs on transmission by An. albimanus was much lower than for An. gambiae. Assuming that people are outside until bedtime, this was similar for the impact of IRS with dichlorodiphenyltrichloroethane (DDT) or bendiocarb, and impact of IRS was less than that of ITNs. However, assuming people go inside when biting starts, IRS had more impact on An. albimanus than ITNs. While house-screening had less impact than ITNs or IRS on An. gambiae, it had more impact on An. albimanus than ITNs or IRS. The impacts of chemoprevention and chemotherapy were comparable in magnitude to those of strategies against An. albimanus. Chemo-prevention impact increased steeply as coverage approached 100%, whilst clinical-case management impact saturated because of remaining asymptomatic infections.

Conclusions

House-screening and repellent IRS are potentially highly effective against An. albimanus if people are indoors during the evening. This is consistent with historical impacts of IRS with DDT, which can be largely attributed to excito-repellency. It also supports the idea that housing improvements have played a critical role in malaria control in North America. For elimination planning, impact estimates need to be combined with feasibility and cost-analysis.
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Literature
1.
go back to reference Sinka ME, Rubio-Palis Y, Manguin S, Patil AP, Temperley WH, Gething PW, et al. The dominant Anopheles vectors of human malaria in the Americas: occurrence data, distribution maps and bionomic precis. Parasit Vectors. 2010;3:72.CrossRef Sinka ME, Rubio-Palis Y, Manguin S, Patil AP, Temperley WH, Gething PW, et al. The dominant Anopheles vectors of human malaria in the Americas: occurrence data, distribution maps and bionomic precis. Parasit Vectors. 2010;3:72.CrossRef
2.
go back to reference Frederick J, Saint JY, Lemoine JF, Dotson EM, Mace KE, Chang M, et al. Malaria vector research and control in Haiti: a systematic review. Malar J. 2016;15:376.CrossRef Frederick J, Saint JY, Lemoine JF, Dotson EM, Mace KE, Chang M, et al. Malaria vector research and control in Haiti: a systematic review. Malar J. 2016;15:376.CrossRef
3.
go back to reference Sinka ME, Bangs MJ, Manguin S, Coetzee M, Mbogo CM, Hemingway J, et al. The dominant Anopheles vectors of human malaria in Africa, Europe and the Middle East: occurrence data, distribution maps and bionomic precis. Parasit Vectors. 2010;3:117.CrossRef Sinka ME, Bangs MJ, Manguin S, Coetzee M, Mbogo CM, Hemingway J, et al. The dominant Anopheles vectors of human malaria in Africa, Europe and the Middle East: occurrence data, distribution maps and bionomic precis. Parasit Vectors. 2010;3:117.CrossRef
4.
go back to reference WHO. World Malaria Report 2017. Geneva, World Health Organization, 2017. WHO. World Malaria Report 2017. Geneva, World Health Organization, 2017.
5.
go back to reference Garrett-Jones C. Prognosis for interruption of malaria transmission through assessment of the mosquito’s vectorial capacity. Nature. 1964;204:1173–5.CrossRef Garrett-Jones C. Prognosis for interruption of malaria transmission through assessment of the mosquito’s vectorial capacity. Nature. 1964;204:1173–5.CrossRef
6.
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
7.
go back to reference Allen LJS. Some discrete-time SI, SIR, and SIS epidemic models. Math Biosci. 1994;124:83–105.CrossRef Allen LJS. Some discrete-time SI, SIR, and SIS epidemic models. Math Biosci. 1994;124:83–105.CrossRef
8.
go back to reference Koella JC. On the use of mathematical models of malaria transmission. Acta Trop. 1991;49:1–25.CrossRef Koella JC. On the use of mathematical models of malaria transmission. Acta Trop. 1991;49:1–25.CrossRef
9.
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
10.
go back to reference Pinault LL, Hunter FF. Characterization of larval habitats of Anopheles albimanus, Anopheles pseudopunctipennis, Anopheles punctimacula, and Anopheles oswaldoi s.l. populations in lowland and highland Ecuador. J Vector Ecol. 2012;37:124–36.CrossRef Pinault LL, Hunter FF. Characterization of larval habitats of Anopheles albimanus, Anopheles pseudopunctipennis, Anopheles punctimacula, and Anopheles oswaldoi s.l. populations in lowland and highland Ecuador. J Vector Ecol. 2012;37:124–36.CrossRef
11.
go back to reference Wagman JM, Grieco JP, Bautista K, Polanco J, Briceno I, King R, et al. The field evaluation of a push-pull system to control malaria vectors in northern Belize, Central America. Malar J. 2015;14:184.CrossRef Wagman JM, Grieco JP, Bautista K, Polanco J, Briceno I, King R, et al. The field evaluation of a push-pull system to control malaria vectors in northern Belize, Central America. Malar J. 2015;14:184.CrossRef
12.
go back to reference Eyles DE, Young M. The duration of untreated or inadequately treated Plasmodium falciparum infections in the human host. J Natl Malar Soc. 1951;10:327–36.PubMed Eyles DE, Young M. The duration of untreated or inadequately treated Plasmodium falciparum infections in the human host. J Natl Malar Soc. 1951;10:327–36.PubMed
13.
go back to reference Sama W, Dietz K, Smith T. Distribution of survival times of deliberate Plasmodium falciparum infections in tertiary syphilis patients. Trans R Soc Trop Med Hyg. 2006;100:811–6.CrossRef Sama W, Dietz K, Smith T. Distribution of survival times of deliberate Plasmodium falciparum infections in tertiary syphilis patients. Trans R Soc Trop Med Hyg. 2006;100:811–6.CrossRef
14.
go back to reference Taylor RT. The ecology of Anopheles albimanus (Wied.) in Haiti. Mosquito News 1966;26: 393-7. Taylor RT. The ecology of Anopheles albimanus (Wied.) in Haiti. Mosquito News 1966;26: 393-7.
15.
go back to reference Desenfant P. Rôle et bioécologie de A. albimanus (Wiedemann, 1820) vecteur du paludisme en Haiti. Université de Paris-Sud; 1988. Desenfant P. Rôle et bioécologie de A. albimanus (Wiedemann, 1820) vecteur du paludisme en Haiti. Université de Paris-Sud; 1988.
16.
go back to reference Knutson KL. Sleep duration, quality, and timing and their associations with age in a community without electricity in Haiti. Am J Hum Biol. 2014;26:80–6.CrossRef Knutson KL. Sleep duration, quality, and timing and their associations with age in a community without electricity in Haiti. Am J Hum Biol. 2014;26:80–6.CrossRef
17.
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.CrossRef 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.CrossRef
18.
go back to reference Govella NJ, Okumu FO, Killeen GF. Insecticide-treated nets can reduce malaria transmission by mosquitoes which feed outdoors. Am J Trop Med Hyg. 2010;82:415–9.CrossRef Govella NJ, Okumu FO, Killeen GF. Insecticide-treated nets can reduce malaria transmission by mosquitoes which feed outdoors. Am J Trop Med Hyg. 2010;82:415–9.CrossRef
19.
go back to reference Charlwood JD, Birley MH, Dagoro H, Paru R, Holmes PR. Assessing survival rates of Anopheles farauti (Diptera, Culicidae) from Papua-New-Guinea. J Anim Ecol. 1985;54:1003–16.CrossRef Charlwood JD, Birley MH, Dagoro H, Paru R, Holmes PR. Assessing survival rates of Anopheles farauti (Diptera, Culicidae) from Papua-New-Guinea. J Anim Ecol. 1985;54:1003–16.CrossRef
20.
go back to reference Moshkovsky SD. The dependence on temperature of the speed of development of malaria Plasmodia in the mosquito. Meditsinkaya Parazitologiya iParazitarnie Bolezni. 1946;15:19 (in Russian). Moshkovsky SD. The dependence on temperature of the speed of development of malaria Plasmodia in the mosquito. Meditsinkaya Parazitologiya iParazitarnie Bolezni. 1946;15:19 (in Russian).
21.
go back to reference Kirby MJ, Ameh D, Bottomley C, Green C, Jawara M, Milligan PJ, et al. Effect of two different house screening interventions on exposure to malaria vectors and on anaemia in children in The Gambia: a randomised controlled trial. Lancet. 2009;374:998–1009.CrossRef Kirby MJ, Ameh D, Bottomley C, Green C, Jawara M, Milligan PJ, et al. Effect of two different house screening interventions on exposure to malaria vectors and on anaemia in children in The Gambia: a randomised controlled trial. Lancet. 2009;374:998–1009.CrossRef
22.
go back to reference RTS SCTP. Efficacy and safety of RTS,S/AS01 malaria vaccine with or without a booster dose in infants and children in Africa: final results of a phase 3, individually randomised, controlled trial. Lancet 2015;386:31–45.CrossRef RTS SCTP. Efficacy and safety of RTS,S/AS01 malaria vaccine with or without a booster dose in infants and children in Africa: final results of a phase 3, individually randomised, controlled trial. Lancet 2015;386:31–45.CrossRef
23.
go back to reference Penny MA, Pemberton-Ross P, Smith TA. The time-course of protection of the RTS, S vaccine against malaria infections and clinical disease. Malar J. 2015;14:437.CrossRef Penny MA, Pemberton-Ross P, Smith TA. The time-course of protection of the RTS, S vaccine against malaria infections and clinical disease. Malar J. 2015;14:437.CrossRef
24.
go back to reference Crowell V, Hardy D, Briet O, Chitnis N, Maire N, Smith T. Can we depend on case management to prevent re-establishment of P. falciparum malaria, after local interruption of transmission? Epidemics. 2012;4:1–8.CrossRef Crowell V, Hardy D, Briet O, Chitnis N, Maire N, Smith T. Can we depend on case management to prevent re-establishment of P. falciparum malaria, after local interruption of transmission? Epidemics. 2012;4:1–8.CrossRef
25.
go back to reference Lindo JF, Bryce JH, DuCasse MB, Howitt C, Barrett DM, Lorenzo MJ, et al. Plasmodium malariae in Haitian refugees, Jamaica. Emerg Infect Dis. 2007;13:931–3.CrossRef Lindo JF, Bryce JH, DuCasse MB, Howitt C, Barrett DM, Lorenzo MJ, et al. Plasmodium malariae in Haitian refugees, Jamaica. Emerg Infect Dis. 2007;13:931–3.CrossRef
26.
go back to reference Weppelmann TA, von Fricken ME, Lam B, Telisma T, Existe A, Lemoine JF, et al. Sparse serological evidence of Plasmodium vivax transmission in the Ouest and Sud-Est departments of Haiti. Acta Trop. 2016;162:27–34.CrossRef Weppelmann TA, von Fricken ME, Lam B, Telisma T, Existe A, Lemoine JF, et al. Sparse serological evidence of Plasmodium vivax transmission in the Ouest and Sud-Est departments of Haiti. Acta Trop. 2016;162:27–34.CrossRef
27.
go back to reference Brady OJ, Slater HC, Pemberton-Ross P, Wenger E, Maude RJ, Ghani AC, et al. Role of mass drug administration in elimination of Plasmodium falciparum malaria: a consensus modelling study. Lancet Glob Health. 2017;5:e680–7.CrossRef Brady OJ, Slater HC, Pemberton-Ross P, Wenger E, Maude RJ, Ghani AC, et al. Role of mass drug administration in elimination of Plasmodium falciparum malaria: a consensus modelling study. Lancet Glob Health. 2017;5:e680–7.CrossRef
28.
go back to reference World Health Organization. Interim Position Statement: The role of larviciding for malaria control in sub-Saharan Africa. Geneva: World Health Organization; 2012. World Health Organization. Interim Position Statement: The role of larviciding for malaria control in sub-Saharan Africa. Geneva: World Health Organization; 2012.
29.
go back to reference Torres-Estrada JL, Meza-Alvarez RA, Cibrian-Tovar J, Rodriguez-Lopez MH, Arredondo-Jimenez JI, Cruz-Lopez L, et al. Vegetation-derived cues for the selection of oviposition substrates by Anopheles albimanus under laboratory conditions. J Am Mosq Control Assoc. 2005;21:344–9.CrossRef Torres-Estrada JL, Meza-Alvarez RA, Cibrian-Tovar J, Rodriguez-Lopez MH, Arredondo-Jimenez JI, Cruz-Lopez L, et al. Vegetation-derived cues for the selection of oviposition substrates by Anopheles albimanus under laboratory conditions. J Am Mosq Control Assoc. 2005;21:344–9.CrossRef
30.
go back to reference Hardy A, Makame M, Cross D, Majambere S, Msellem M. Using low-cost drones to map malaria vector habitats. Parasit Vectors. 2017;10:29.CrossRef Hardy A, Makame M, Cross D, Majambere S, Msellem M. Using low-cost drones to map malaria vector habitats. Parasit Vectors. 2017;10:29.CrossRef
31.
go back to reference Tusting LS, Ippolito MM, Willey BA, Kleinschmidt I, Dorsey G, Gosling RD, et al. The evidence for improving housing to reduce malaria: a systematic review and meta-analysis. Malar J. 2015;14:209.CrossRef Tusting LS, Ippolito MM, Willey BA, Kleinschmidt I, Dorsey G, Gosling RD, et al. The evidence for improving housing to reduce malaria: a systematic review and meta-analysis. Malar J. 2015;14:209.CrossRef
32.
go back to reference Celli A. The new prophylaxis against malaria: an account of experiments in Latium. Lancet. 1900;156:1603–6.CrossRef Celli A. The new prophylaxis against malaria: an account of experiments in Latium. Lancet. 1900;156:1603–6.CrossRef
33.
go back to reference Lindsay SW, Emerson PM, Charlwood JD. Reducing malaria by mosquito-proofing houses. Trends Parasitol. 2002;18:510–4.CrossRef Lindsay SW, Emerson PM, Charlwood JD. Reducing malaria by mosquito-proofing houses. Trends Parasitol. 2002;18:510–4.CrossRef
36.
go back to reference Steinhardt LC, Jean YS, Impoinvil D, Mace KE, Wiegand R, Huber CS, et al. Effectiveness of insecticide-treated bednets in malaria prevention in Haiti: a case-control study. Lancet Glob Health. 2017;5:e96–103.CrossRef Steinhardt LC, Jean YS, Impoinvil D, Mace KE, Wiegand R, Huber CS, et al. Effectiveness of insecticide-treated bednets in malaria prevention in Haiti: a case-control study. Lancet Glob Health. 2017;5:e96–103.CrossRef
37.
go back to reference Bangs MJ. The susceptibility and behavioral response of Anopheles albimanus Weidemann and Anopheles vestitipennis Dyar and Knab (Diptera: Culicidae) to insecticides in northern Belize, Central America. Ann Arbor: University of Michigan; 1999. Bangs MJ. The susceptibility and behavioral response of Anopheles albimanus Weidemann and Anopheles vestitipennis Dyar and Knab (Diptera: Culicidae) to insecticides in northern Belize, Central America. Ann Arbor: University of Michigan; 1999.
38.
go back to reference Dusfour I, Achee NL, Roberts DR. Grieco JP Contact irritancy and spatial repellency behaviors in Anopheles albimanus Wiedemann (Diptera: Culicidae) collected in Orange Walk, Belize, C.A. J Vector Ecol. 2009;34:232–7.CrossRef Dusfour I, Achee NL, Roberts DR. Grieco JP Contact irritancy and spatial repellency behaviors in Anopheles albimanus Wiedemann (Diptera: Culicidae) collected in Orange Walk, Belize, C.A. J Vector Ecol. 2009;34:232–7.CrossRef
39.
go back to reference Roberts DR, Alecrim WD, Hshieh P, Grieco JP, Bangs M, Andre RG, et al. A probability model of vector behavior: effects of DDT repellency, irritancy, and toxicity in malaria control. J Vector Ecol. 2000;25:48–61.PubMed Roberts DR, Alecrim WD, Hshieh P, Grieco JP, Bangs M, Andre RG, et al. A probability model of vector behavior: effects of DDT repellency, irritancy, and toxicity in malaria control. J Vector Ecol. 2000;25:48–61.PubMed
40.
go back to reference Waite JL, Swain S, Lynch PA, Sharma SK, Haque MA, Montgomery J, et al. Increasing the potential for malaria elimination by targeting zoophilic vectors. Sci Rep. 2017;7:40551.CrossRef Waite JL, Swain S, Lynch PA, Sharma SK, Haque MA, Montgomery J, et al. Increasing the potential for malaria elimination by targeting zoophilic vectors. Sci Rep. 2017;7:40551.CrossRef
41.
go back to reference Che-Mendoza A, Guillermo-May G, Herrera-Bojorquez J, Barrera-Perez M, Dzul-Manzanilla F, Gutierrez-Castro C, et al. Long-lasting insecticide-treated house screens and targeted treatment of productive breeding-sites for dengue vector control in Acapulco, Mexico. Trans R Soc Trop Med Hyg. 2015;109:106–15.CrossRef Che-Mendoza A, Guillermo-May G, Herrera-Bojorquez J, Barrera-Perez M, Dzul-Manzanilla F, Gutierrez-Castro C, et al. Long-lasting insecticide-treated house screens and targeted treatment of productive breeding-sites for dengue vector control in Acapulco, Mexico. Trans R Soc Trop Med Hyg. 2015;109:106–15.CrossRef
42.
go back to reference Mekuria Y, Granados R, Tidwell MA, Williams DC, Wirtz RA. Roberts DR Malaria transmission potential by Anopheles mosquitoes of Dajabon, Dominican Republic. J Am Mosq Control Assoc. 1991;7:456–61.PubMed Mekuria Y, Granados R, Tidwell MA, Williams DC, Wirtz RA. Roberts DR Malaria transmission potential by Anopheles mosquitoes of Dajabon, Dominican Republic. J Am Mosq Control Assoc. 1991;7:456–61.PubMed
43.
go back to reference Molez JF, Desenfant P, Jacques JR. Bio-ecology of Anopheles albimanus Wiedeman, 1820 (Diptera: Culicidae) in Haiti (Hispaniola). Bull Soc Pathol Exot. 1998;91:334–9.PubMed Molez JF, Desenfant P, Jacques JR. Bio-ecology of Anopheles albimanus Wiedeman, 1820 (Diptera: Culicidae) in Haiti (Hispaniola). Bull Soc Pathol Exot. 1998;91:334–9.PubMed
44.
go back to reference Killeen GF, Kihonda J, Lyimo E, Oketch FR, Kotas ME, Mathenge E, et al. Quantifying behavioural interactions between humans and mosquitoes: evaluating the protective efficacy of insecticidal nets against malaria transmission in rural Tanzania. BMC Infect Dis. 2006;6:161.CrossRef Killeen GF, Kihonda J, Lyimo E, Oketch FR, Kotas ME, Mathenge E, et al. Quantifying behavioural interactions between humans and mosquitoes: evaluating the protective efficacy of insecticidal nets against malaria transmission in rural Tanzania. BMC Infect Dis. 2006;6:161.CrossRef
Metadata
Title
Models of effectiveness of interventions against malaria transmitted by Anopheles albimanus
Authors
Olivier J. T. Briët
Daniel E. Impoinvil
Nakul Chitnis
Emilie Pothin
Jean Frantz Lemoine
Joseph Frederic
Thomas A. Smith
Publication date
01-12-2019
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2019
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-019-2899-3

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