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The entomological inoculation rate and Plasmodium falciparum infection in African children

Abstract

Malaria is an important cause of global morbidity and mortality. The fact that some people are bitten more often than others has a large effect on the relationship between risk factors and prevalence of vector-borne diseases1,2,3. Here we develop a mathematical framework that allows us to estimate the heterogeneity of infection rates from the relationship between rates of infectious bites and community prevalence. We apply this framework to a large, published data set that combines malaria measurements from more than 90 communities4. We find strong evidence that heterogeneous biting or heterogeneous susceptibility to infection are important and pervasive factors determining the prevalence of infection: 20% of people receive 80% of all infections. We also find that individual infections last about six months on average, per infectious bite, and children who clear infections are not immune to new infections. The results have important implications for public health interventions: the success of malaria control will depend heavily on whether efforts are targeted at those who are most at risk of infection.

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Figure 1: The data and fitted functions and a sensitivity analysis for the best overall model.

References

  1. Dietz, K. Models for vector-borne parasitic diseases. Lecture Notes Biomath. 39, 264–277 (1980)

    MathSciNet  Article  Google Scholar 

  2. Dye, C. & Hasibeder, G. Population dynamics of mosquito-borne disease: effects of flies which bite some people more frequently than others. Trans. Soc. Trop. Med. Hyg. 80, 69–77 (1986)

    CAS  Article  Google Scholar 

  3. Woolhouse, M. E. et al. Heterogeneities in the transmission of infectious agents: implications for the design of control programs. Proc. Natl Acad. Sci. USA 94, 338–342 (1997)

    ADS  CAS  Article  Google Scholar 

  4. Hay, S. I., Guerra, C. A., Tatem, A. J., Atkinson, P. M. & Snow, R. W. Urbanization, malaria transmission, and disease burden in Africa. Nature Rev. Microbiol. 3, 81–90 (2005)

    CAS  Article  Google Scholar 

  5. Hay, S. I., Guerra, C. A., Tatem, A. J., Noor, A. M. & Snow, R. W. The global distribution and population at risk of malaria: past, present and future. Lancet Infect. Dis. 4, 327–336 (2004)

    Article  Google Scholar 

  6. Snow, R. W., Guerra, C. A., Noor, A. M., Myint, H. Y. & Hay, S. I. The global distribution of clinical episodes of Plasmodium falciparum malaria. Nature 434, 214–217 (2005)

    ADS  CAS  Article  Google Scholar 

  7. Murray, C. J. L. & Lopez, A. D. Alternative projections of mortality and disability by cause 1990–2020: Global burden of disease study. Lancet 24,1498–1504 (1997)

    Article  Google Scholar 

  8. Jamison, D. T., Creese, A. & Prentice, T. World Health Report, 1999: Making a Difference (World Health Organization, Geneva, 1999)

    Google Scholar 

  9. Snow, R. W. & Gilles, H. M. in Essential Malariology 4th edn (eds Warrell, D. A. & Gilles, H. M.) Ch. 5, 85–106 (Arnold, London, 2002)

    Google Scholar 

  10. Snow, R. W. & Marsh, K. The consequences of reducing transmission of Plasmodium falciparum in Africa. Adv. Parasitol. 52, 235–264 (2002)

    Article  Google Scholar 

  11. Macdonald, G. The Epidemiology and Control of Malaria (Oxford Univ. Press, London, 1957)

    Google Scholar 

  12. Ross, R. The Prevention of Malaria (John Murray, London, 1911)

    Google Scholar 

  13. Nájera, J. A. A critical review of the field application of a mathematical model of malaria eradication. Bull. World Health Organ. 50, 449–457 (1974)

    PubMed  PubMed Central  Google Scholar 

  14. Smith, D. L., Dushoff, J. & McKenzie, F. E. The risk of a mosquito-borne infection in a heterogeneous environment. PLoS Biol. 2, e368 (2004)

    Article  Google Scholar 

  15. Takken, W. & Knols, B. G. J. Odor-mediated behaviour of Afrotropical malaria mosquitoes. Annu. Rev. Entomol. 44, 131–157 (1999)

    CAS  Article  Google Scholar 

  16. Hethcote, H. W. & Yorke, J. A. In Lecture Notes in Biomathematics Vol. 56, 1–105 (Springer, Berlin, 1984)

    Google Scholar 

  17. Walton, G. A. On the control of Malaria in Freetown, Sierra Leone. I. Plasmodium falciparum and Anopheles gambiae in relation to malaria occurring in infants. Ann. Trop. Med. Parasitol. 41, 380–407 (1947)

    CAS  Article  Google Scholar 

  18. Dietz, K., Molineaux, L. & Thomas, A. A malaria model tested in the African savannah. Bull. World Health Organ. 50, 347–357 (1974)

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Aron, J. L. & May, R. M. in Population Dynamics and Infectious Disease (ed. Anderson, R. M.) Ch. 5, 139–179 (Chapman and Hall, London, 1982)

    Book  Google Scholar 

  20. Bailey, N. T. J. The Biomathematics of Malaria (Oxford Univ. Press, Oxford, 1982)

    MATH  Google Scholar 

  21. McKenzie, F. E., Sirichaisinthop, J., Miller, R. S., Gasser, R. A. & Wongsrichanalai, C. Jr Dependence of malaria detection and species diagnosis by microscopy on parasite density. Am. J. Trop. Med. Hyg. 69, 372–376 (2003)

    Article  Google Scholar 

  22. R Development Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, Vienna, Austria, 2004); http://www.R-project.org.3-900051-07-0

  23. Beier, J. C., Killeen, G. F. & Githure, J. I. Short report: entomologic inoculation rates and Plasmodium falciparum malaria prevalence in Africa. Am. J. Trop. Med. Hyg. 61, 109–113 (1999)

    CAS  Article  Google Scholar 

  24. Burnham, K. P. & Anderson, D. A. Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach 2nd edn (Springer, New York, 2002)

    MATH  Google Scholar 

  25. Eyles, D. E. & Young, M. D. The duration of untreated or inadequately treated Plasmodium falciparum infections in the human host. J. Nat. Malaria Soc. 10, 327–336 (1951)

    CAS  PubMed  Google Scholar 

  26. Gu, W. et al. Low recovery rates stabilize malaria endemicity in areas of low transmission in coastal Kenya. Acta Trop. 86, 71–81 (2003)

    Article  Google Scholar 

  27. Sama, W., Killeen, G. & Smith, T. Estimating the duration of Plasmodium falciparum infection from trials of indoor residual spraying. Am. J. Trop. Med. Hyg. 70, 625–634 (2004)

    Article  Google Scholar 

  28. Bagster Wilson, D. Rural hyperendemic malaria in Tanganyika Territory. Trans. R. Soc. Trop. Med. Hyg. 29, 583–618 (1936)

    Article  Google Scholar 

  29. Molineaux, L. & Gramiccia, G. The Garki Project (World Health Organization, Geneva, 1980)

    Google Scholar 

Download references

Acknowledgements

We thank D. Bradley, B. Grenfell, F. E. McKenzie, W. Prudhomme, S. Randolph, M. Recker, D. Rogers and L. Waller for comments and suggestions. We also thank the NCEAS working group for discussion. S.I.H. is funded by a Research Career Development Fellowship from the Wellcome Trust. R.W.S. is a Wellcome Trust Senior Research Fellow and acknowledges the support of the Kenyan Medical Research Institute (KEMRI). This work was partially conducted as part of the Environment and Disease Working Group supported by the National Center for Ecological Analysis and Synthesis, a Center funded by NSF, the University of California Santa Barbara, and the State of California. The views presented in this Letter represent the personal views of the authors and do not construe or imply any official position or policy of the Fogarty International Center, National Institutes of Health, Department of Health and Human Services, or the US government. Author Contributions S.I.H. collated the data. D.L.S. designed and conducted the analysis. D.L.S., J.D., S.I.H. and R.W.S. wrote the paper.

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Smith, D., Dushoff, J., Snow, R. et al. The entomological inoculation rate and Plasmodium falciparum infection in African children. Nature 438, 492–495 (2005). https://doi.org/10.1038/nature04024

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