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Resistance to larvicides in mosquito populations and how it could benefit malaria control

Published online by Cambridge University Press:  20 December 2012

RONGSONG LIU  and
STEPHEN A. GOURLEY
RONGSONG LIU
Affiliation:
Department of Mathematics and Department of Zoology and Physiology, University of Wyoming, Laramie, WY 82071, USA email: [email protected]
STEPHEN A. GOURLEY
Affiliation:
Department of Mathematics, University of Surrey, Guildford, Surrey, GU2 7XH, UK email: [email protected]
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Abstract

We model larviciding of mosquitoes taking into account the evolution of resistance to the larvicides, the evolutionary costs of resistance and the implications for malaria control. There is evidence that resistance comes with various costs, one of which is reduced adult longevity for resistant mutants. The mosquito adult lifespan is one of the most crucial parameters in malaria transmission due to a long developmental time for the malaria parasite in the insect. A possible malaria control strategy is therefore to shorten this adult lifespan by larviciding with a potent larvicide to which mosquitoes become resistant. This novel strategy is studied using a mathematical model for the wild type and resistant mutants and by incorporating the malaria disease dynamics using an SEI type model with standard incidence that incorporates the latency period of the parasite in wild-type and resistant mosquitoes. We consider the linear stability of the malaria-free equilibrium in which the resistant strain is dominant and derive a condition for the global eradication of malaria. Numerical simulations are presented, which offer further insights. The parameter to which the analysis is most sensitive is the per-capita death rate of resistant adult mosquitoes. Increasing this parameter dramatically reduces the basic reproduction number R0. However, increasing it too much causes the wild type to outcompete the resistant mutants, and the control strategy fails. Exploitation of costs of resistance to larvicides thus offers a possible malaria control measure if the larvicide is sufficiently potent and costs of resistance are neither too great nor too small.

Keywords

MosquitoLarvicideEvolutionMalariaDelayStability
Type
Papers
Information
European Journal of Applied Mathematics , Volume 24 , Issue 3 , June 2013 , pp. 415 - 436
Copyright
Copyright © Cambridge University Press 2012

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References

[1]Bargielowski, I. & Koella, J. C. (2009) A possible mechanism for the suppression of Plasmodium berghei development in the mosquito Anopheles gambiae by the microsporidian Vavraia culicis. PLoS One 4, e4676.CrossRefGoogle ScholarPubMed
[2]Centers for Disease Control (CDC), Anopheles mosquitoes. Accessed 18 August 2011. URL: http://www.cdc.gov/malaria/about/biology/mosquitoes/index.html.Google Scholar
[3]Centers for Disease Control (CDC), Malaria. Accessed 18 August 2011. URL: http://www.cdc.gov/malaria/about/disease.html.Google Scholar
[4]Charlwood, J. D., Smith, T., Billingsley, P. F., Takken, W., Lyimo, E. O. K. & Meuwissen, J. H. E. T. (1997) Survival and infection probabilities of anthropophagic anophelines from an area of high prevalence of Plasmodium falciparum in humans. Bull. Entomol. Res. 87, 445–453.CrossRefGoogle Scholar
[5]Chitnis, N., Cushing, J. M. & Hyman, J. M. (2007) Bifurcation analysis of a mathematical model for malaria transmission. SIAM J. Appl. Math. 67, 24–45.CrossRefGoogle Scholar
[6]Chitnis, N., Hyman, J. M. & Cushing, J. M. (2008) Determining important parameters in the spread of malaria through the sensitivity analysis of a mathematical model. Bull. Math. Biol. 70, 1272–1296.CrossRefGoogle ScholarPubMed
[7]Gazave, E., Chevillon, C., Lenormand, T., Marquine, M. & Raymond, M. (2001) Dissecting the cost of insecticide resistance genes during the overwintering period of the mosquito Culex pipiens. Heredity 87, 441–448.CrossRefGoogle ScholarPubMed
[8]Gourley, S. A., Liu, R. & Wu, J. (2011) Slowing the evolution of insecticide resistance in mosquitoes: A mathematical model. Proc. Roy. Soc. Lond., Ser. A 467, 2127–2148.Google Scholar
[9]Gurney, W. S. C., Blythe, S. P. & Nisbet, R. M. (1980) Nicholson's blowflies revisited. Nature 287, 17–21.CrossRefGoogle Scholar
[10]Hale, J. (1977) Theory of Functional Differential Equations, Springer-Verlag, New York.CrossRefGoogle Scholar
[11]Hemingway, J., Field, L. & Vontas, J. (2002) An overview of insecticide resistance. Science 298, 96–97.CrossRefGoogle ScholarPubMed
[12]Hemingway, J., Hawkes, N. J., McCarroll, L. & Ranson, H. (2004) The molecular basis of insecticide resistance in mosquitoes. Insect Biochem. Mol. Biol. 34, 653–65.CrossRefGoogle ScholarPubMed
[13]Kelly-Hope, L., Ranson, H. & Hemingway, J. (2008) Lessons from the past: Managing insecticide resistance in malaria control and eradication programmes. Lancet Infect. Dis. 8, 387–389.CrossRefGoogle ScholarPubMed
[14]Killeen, G. F., Fillinger, U., Kiche, I., Gouagna, L. C. & Knols, B. G. (2002) Eradication of Anopheles gambiae from Brazil: Lessons for malaria control in Africa? Lancet Infect. Dis. 2, 618–627.CrossRefGoogle ScholarPubMed
[15]Killeen, G. F., Fillinger, U. & Knols, B. G. J. (2002) Advantages of larval control for African malaria vectors: Low mobility and behavioural responsiveness of immature mosquito stages allow high effective coverage. Malaria J. 1, 8.CrossRefGoogle ScholarPubMed
[16]Killeen, G. F., McKenzie, F. E., Foy, B. D., Schieffelin, C., Billingsley, P. F. & Beier, J. C. (2000) A simplified model for predicting malaria entomologic inoculation rates based on entomologic and parasitologic parameters relevant to control. Am. J. Trop. Med. Hyg. 62, 535–544.CrossRefGoogle ScholarPubMed
[17]Koella, J. C., Lynch, P. A., Thomas, M. B. & Read, A. F. (2009) Towards evolution-proof malaria control with insecticides. Evol. Appl. 2, 469–480.CrossRefGoogle ScholarPubMed
[18]Koella, J. C., Rieu, L. & Paul, R. E. L. (2002) Stage-Specific manipulation of a mosquito's host-seeking behavior by the malaria parasite Plasmodium gallinaceum. Behav. Ecol. 13, 816–820.CrossRefGoogle Scholar
[19]Kuang, Y. (1993) Delay Differential Equations: With Applications in Population Dynamics. Mathematics in Science and Engineering series, Vol. 191, Academic Press, Boston, MA.Google Scholar
[20]Lehmann, T., Dalton, R., Kim, E. H., Dahl, E., Diabate, A., Dabire, R. & Dujardin, J. P. (2006) Genetic contribution to variation in larval development time, adult size, and longevity of starved adults of Anopheles gambiae. Infect. Genet. Evol. 6, 410–416.CrossRefGoogle ScholarPubMed
[21]Macdonald, G. (1957) The Epidemiology and Control of Malaria, Oxford University Press, London.Google Scholar
[22]Read, A. F., Lynch, P. A. & Thomas, M. B. (2009) How to make evolution-proof insecticides for malaria control. PLoS Biol. 7 (4), e1000058. doi:10.1371/journal.pbio.1000058.CrossRefGoogle ScholarPubMed
[23]Ruan, S., Xiao, D. & Beier, J. C. (2008) On the delayed Ross–Macdonald model for malaria transmission. Bull. Math. Biol. 70, 1098–1114.CrossRefGoogle ScholarPubMed
[24]Shousha, A. T. (1948) Species eradication. The eradication of Anopheles gambiae from Upper Egypt, 1942–1945. Bull. Wld. Hlth. Org. 1, 309–353.Google ScholarPubMed
[25]Silver, J. B. (2008) Mosquito Ecology: Field Sampling Methods, Springer, New York.CrossRefGoogle Scholar
[26]Smith, H. L. (1995) Monotone Dynamical Systems. An Introduction to the Theory of Competitive and Cooperative Systems. Mathematical Surveys and Monographs, 41. American Mathematical Society, Providence, RI.Google Scholar
[27]Soper, F. L. & Wilson, D. B. (1943) Anopheles Gambiae in Brazil: 1930 to 1940, The Rockefeller Foundation: New York.Google Scholar
[28]Thomas, M. B. & Read, A. F. (2007) Can fungal biopesticides control malaria? Nat. Rev. Microbiol. 5, 377–383.CrossRefGoogle ScholarPubMed
[29]Utzinger, J., Tozan, Y. & Singer, B. H. (2001) Efficacy and cost-effectiveness of environmental management for malaria control. Trop. Med. Int. Health. 6, 677–687.CrossRefGoogle ScholarPubMed
[30]Webb, G. F., D'Agata, E. M. C., Magal, P. & Ruan, S. (2005) A model of antibiotic-resistant bacterial epidemics in hospitals. Proc. Nat. Acad. Sci. USA 102, 13343–13348.CrossRefGoogle Scholar
[31]Wonham, M. J., de-Camino-Beck, T. & Lewis, M. A. (2004) An epidemiological model for West Nile virus: Invasion analysis and control applications. Proc. R. Soc. Lond. Ser. B. 271, 501–507.CrossRefGoogle ScholarPubMed
[32]World Health Organisation (2012) The Role of Larviciding for Malaria Control in Sub-Saharan Africa (Interim Position Statement), World Health Organisation, Geneva, Switzerland.Google Scholar
[33]Worrall, E. & Fillinger, U. (2011) Large-scale use of mosquito larval source management for malaria control in Africa: A cost analysis. Malaria J. 10, 338.CrossRefGoogle ScholarPubMed