The online version of this article (doi:10.1186/1475-2875-11-383) contains supplementary material, which is available to authorized users.
The authors declare that they have no competing interests.
PL developed and applied the model and contributed to study inception, interpretation of results and drafting of the manuscript. UG reviewed the model and contributed to drafting of the manuscript. MT and AR contributed to study inception, interpretation of results and drafting of the manuscript. All authors read and approved the final manuscript.
Chemical insecticides against adult mosquitoes are a key element in most malaria management programmes, but their efficacy is threatened by the evolution of insecticide-resistant mosquitoes. By killing only older mosquitoes, entomopathogenic fungi can in principle significantly impact parasite transmission while imposing much less selection for resistance. Here an assessment is made as to which of the wide range of possible virulence characteristics for fungal biopesticides best realise this potential.
With mathematical models that capture relevant timings and survival probabilities within successive feeding cycles, transmission and resistance-management metrics are used to compare susceptible and resistant mosquitoes exposed to no intervention, to conventional instant-kill interventions, and to delayed-action biopesticides with a wide range of virulence characteristics.
Fungal biopesticides that generate high rates of mortality at around the time mosquitoes first become able to transmit the malaria parasite offer potential for large reductions in transmission while imposing low fitness costs. The best combinations of control and resistance management are generally accessed at high levels of coverage. Strains which have high virulence in malaria-infected mosquitoes but lower virulence in malaria-free mosquitoes offer the ultimate benefit in terms of minimizing selection pressure whilst maximizing impact on transmission. Exploiting this phenotype should be a target for product development. For indoor residual spray programmes, biopesticides may offer substantial advantages over the widely used pyrethroid-based insecticides. Not only do fungal biopesticides provide substantial resistance management gains in the long term, they may also provide greater reductions in transmission before resistance has evolved. This is because fungal spores do not have contact irritancy, reducing the chances that a blood-fed mosquito can survive an encounter and thus live long enough to transmit malaria.
Delayed-action products, such as fungal biopesticides, have the potential to achieve reductions in transmission comparable with those achieved with existing instant-kill insecticides, and to sustain this control for substantially longer once resistant alleles arise. Given the current insecticide resistance crisis, efforts should continue to fully explore the operational feasibility of this alternative approach.
Additional file 1: Appendix A. Derivation of the feeding cycle model. Detailed description of variables and calculations used in the feeding cycle model. (PDF 173 KB)12936_2012_2533_MOESM1_ESM.pdf
Additional file 2: Appendix B. Derivation of the population model. Detailed description of variables and calculations used in the population model. (PDF 163 KB)12936_2012_2533_MOESM2_ESM.pdf
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Yewhalaw D, Wassie F, Steurbaut W, Spanoghe P, Van Bortel W, Denis L, Tessema DA, Getachew Y, Coosemans M, Duchateau L, Speybroeck N: Multiple insecticide resistance: an impediment to insecticide-based malaria vector control program. PLoS One. 2011, 6: e16066-10.1371/journal.pone.0016066. PubMedCentralCrossRefPubMed
Chanda E, Hemingway J, Kleinschmidt I, Rehman AM, Ramdeen V, Phiri FN, Coetzer S, Mthembu D, Shinondo CJ, Chizema-Kawesha E, Kamuliwo M, Mukonka V, Baboo KS, Coleman M: Insecticide resistance and the future of malaria control in Zambia. PLoS One. 2011, 6: e24336-10.1371/journal.pone.0024336. PubMedCentralCrossRefPubMed
Trape J-F, Tall A, Diagne N, Ndiath O, Ly AB, Faye J, Dieye-Ba F, Roucher C, Bouganali C, Badiane A, Sarr FD, Mazenot C, Touré-Baldé A, Raoult D, Druilhe P, Mercereau-Puijalon O, Rogier C, Sokhna C: Malaria morbidity and pyrethroid resistance after the introduction of insecticide-treated bednets and artemisinin-based combination therapies: a longitudinal study. Lancet Infect Dis. 2011, 11: 925-932. 10.1016/S1473-3099(11)70194-3. CrossRefPubMed
World Health Organisation: World malaria report. 2011, World Health Organisation website. Available at http://www.who.int/malaria/world_malaria_report_2011/en/
Read AF, Lynch PA, Thomas MB: How to make evolution-proof insecticides for malaria control. PLoS Biol. 2009, 7: e58-10.1371/journal.pbio.1000058. CrossRef
Thomas MB, Read AF: Can fungal biopesticides control malaria?. Nat Revs Microbiol. 2007, 5: 377-383. 10.1038/nrmicro1638. CrossRef
Blanford S, Shi W, Christian R, Marden JH, Koekemoer LL, Brooke BD, Coetzee M, Read AF, Thomas MB: Lethal and pre-lethal effects of a fungal biopesticide contribute to substantial and rapid control of malaria vectors. PLoS One. 2011, 6: e23591-10.1371/journal.pone.0023591. PubMedCentralCrossRefPubMed
Farenhorst M, Farina D, Scholte E-J, Takken W, Hunt RH, Coetzee M, Knols BGJ: African water storage pots for the delivery of the entomopathogenic fungus Metarhizium anisopliae to the malaria vectors Anopheles gambiae s.s. and Anopheles funestus. Am J Trop Med Hyg. 2008, 78: 910-916. PubMed
Blanford S, Jenkins NJ, Read AF, Thomas MB: Evaluating the lethal and pre-lethal effect of a range of fungi against adult mosquitoes. Malar J. 2012, in press
Darbro JM, Graham RI, Kay BH, Ryan PA, Thomas MB: Evaluation of entomopathogenic fungi as potential biological control agents of the dengue mosquito, Aedes aegypti (Diptera: Culicidae). Biocontrol Sci. 2011, 21: 1027-1047. 10.1080/09583157.2011.597913. CrossRef
Mandal S, Sarkar R, Sinha S: Mathematical models of malaria - a review. Malar J. 2011, 10: 109-10.1186/1475-2875-10-109. CrossRef
Koella JC, Lynch PA, Thomas MB, Read AF: Towards evolution-proof malaria control with insecticides. Evol App. 2009, 2: 469-480. 10.1111/j.1752-4571.2009.00072.x. CrossRef
Gourley SA, Liu R, Wu J: Slowing the evolution of insecticide resistance in mosquitoes: a mathematical model. Proc R Soc A. 2011, 467: 2127-2148. 10.1098/rspa.2010.0413. CrossRef
Saul AJ, Graves PM, Kay BH: A cyclical feeding model for pathogen transmission and its application to determine vectorial capacity from vector infection-rates. J Appl Ecol. 1990, 27: 123-133. 10.2307/2403572. CrossRef
Killeen GF, Smith TA: Exploring the contributions of bed nets, cattle, insecticides and excitorepellency to malaria control: a deterministic model of mosquito host-seeking behaviour and mortality. Trans R Soc Trop Med Hyg. 2007, 101: 867-880. 10.1016/j.trstmh.2007.04.022. PubMedCentralCrossRefPubMed
Lwetoijera DW, Sumaye RD, Madumla EP, Kavishe DR, Mnyone LL, Russell TL, Okumu FO: An extra-domiciliary method of delivering entomopathogenic fungus, Metharizium anisopliae IP 46 for controlling adult populations of the malaria vector. Anopheles arabiensis. Parasit Vectors. 2010, 3: 18-10.1186/1756-3305-3-18. CrossRefPubMed
Kongmee M, Boonyuan W, Achee NL, Prabaripai A, Lerdthusnee K, Chareonviriyaphap T: Irritant and repellent responses of Anopheles harrisoni and Anopheles minimus upon exposure to bifenthrin or deltamethrin using an excito-repellency system and a live host. J Am Mosq Control Assoc. 2012, 28: 20-29. 10.2987/11-6197.1. CrossRefPubMed
- Prospective malaria control using entomopathogenic fungi: comparative evaluation of impact on transmission and selection for resistance
Penelope A Lynch
Matthew B Thomas
Andrew F Read
- BioMed Central
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