Advertisement

Mathematics of Malaria and Climate Change

  • Steffen E. Eikenberry
  • Abba B. GumelEmail author
Chapter
Part of the Mathematics of Planet Earth book series (MPE, volume 5)

Abstract

This chapter is concerned with malaria and the impact of climate change on the spread of malarial diseases on the African continent. The focus is on mathematical models describing the dynamics of malaria under various climate scenarios. The models fit into the Ross–Macdonald framework, with extensions to incorporate a fuller description of the Anopheles mosquito life cycle and the basic physics of aquatic anopheline microhabitats. Macdonald’s basic reproduction number, \(\mathcal {R}_0\), is used as the primary metric for malaria potential. It is shown that the inclusion of air–water temperature differences significantly affects predicted malaria potential. The chapter includes several maps that relate the local ambient temperature to malaria potential across the continent. Under plausible global warming scenarios, western coastal Africa is likely to see a small decrease in malaria potential, while central, and especially eastern highland Africa, may see an increase in malaria potential.

Keywords

Anopheles mosquito Malaria Ross–Macdonald framework Basic reproduction number Malaria potential Africa 

References

  1. 1.
    Agusto, F., Gumel, A., Parham, P.: Qualitative assessment of the role of temperature variations on malaria transmission dynamics. J. Biol. Syst. 23(4), 597–630 (2015)MathSciNetzbMATHCrossRefGoogle Scholar
  2. 2.
    Allen, R.G., Pereira, L.S., Raes, D., et al.: FAO Crop evapotranspiration (guidelines for computing crop water requirements irrigation and drainage paper 56. Technical Report, Food and Agriculture Organization of the United Nations (FAO), Rome, (1998)Google Scholar
  3. 3.
    Alonso, D., Bouma, M.J., Pascual, M.: Epidemic malaria and warmer temperatures in recent decades in an East African highland. Proc. R. Soc. Lond. B Biol. Sci. 278(1712), 1661–1669 (2010)CrossRefGoogle Scholar
  4. 4.
    Antinori, S., Galimberti, L., Milazzo, L., et al.: Biology of human malaria plasmodia including Plasmodium knowlesi. Mediter. J. Hematol. Infect. Dis. 4(1) (2012)CrossRefGoogle Scholar
  5. 5.
    Asare, E.O., Tompkins, A.M., Amekudzi, L.K., et al.: A breeding site model for regional, dynamical malaria simulations evaluated using in situ temporary ponds observations. Geospat. Health 11(1s), 391 (2016)Google Scholar
  6. 6.
    Asare, E.O., Tompkins, A.M., Amekudzi, L.K., et al.: Mosquito breeding site water temperature observations and simulations towards improved vector-borne disease models for Africa. Geospat. Health 11(1s), 67–77 (2016)Google Scholar
  7. 7.
    Asare, E.O., Tompkins, A.M., Bomblies, A.: A regional model for malaria vector developmental habitats evaluated using explicit, pond-resolving surface hydrology simulations. PLoS One 11(3), e0150626 (2016)CrossRefGoogle Scholar
  8. 8.
    Bayoh, M.N.: Studies on the Development and Survival of Anopheles Gambiae Sensu Stricto at Various Temperatures and Relative Humidities. Ph.D. thesis, Durham University, Durham (2001). http://etheses.dur.ac.uk/4952/
  9. 9.
    Bayoh, M., Lindsay, S.: Effect of temperature on the development of the aquatic stages of Anopheles gambiae sensu stricto (diptera: Culicidae). Bull. Entomol. Res. 93(5), 375–381 (2003)CrossRefGoogle Scholar
  10. 10.
    Bayoh, M.N., Lindsay, S.W.: Temperature-related duration of aquatic stages of the Afrotropical malaria vector mosquito Anopheles gambiae in the laboratory. Med. Vet. Entomol. 18(2), 174–179 (2004)CrossRefGoogle Scholar
  11. 11.
    Beck-Johnson, L.M., Nelson, W.A., Paaijmans, K.P., et al.: The effect of temperature on anopheles mosquito population dynamics and the potential for malaria transmission. PLoS One 8(11), e79276 (2013)CrossRefGoogle Scholar
  12. 12.
    Beck-Johnson, L.M., Nelson, W.A., Paaijmans, K.P., et al.: The importance of temperature fluctuations in understanding mosquito population dynamics and malaria risk. R. Soc. Open Sci. 4(3), 160969 (2017)CrossRefGoogle Scholar
  13. 13.
    Bhatt, S., Weiss, D., Cameron, E., et al.: The effect of malaria control on Plasmodium falciparum in Africa between 2000 and 2015. Nature 526(7572), 207–211 (2015)CrossRefGoogle Scholar
  14. 14.
    Blanford, J.I., Blanford, S., Crane, R.G., et al.: Implications of temperature variation for malaria parasite development across Africa. Sci. Rep. 3, 1300 (2013)CrossRefGoogle Scholar
  15. 15.
    Bomblies, A.: Modeling the role of rainfall patterns in seasonal malaria transmission. Clim. Chang. 112(3–4), 673–685 (2012)CrossRefGoogle Scholar
  16. 16.
    Bomblies, A., Duchemin, J.B., Eltahir, E.A.: Hydrology of malaria: model development and application to a Sahelian village. Water Resour. Res. 44(12) (2008)Google Scholar
  17. 17.
    Briere, J.F., Pracros, P., Le Roux, A.Y., et al.: A novel rate model of temperature-dependent development for arthropods. Environ. Entomol. 28(1), 22–29 (1999)CrossRefGoogle Scholar
  18. 18.
    Briët, O.J., Vounatsou, P., Gunawardena, D.M., et al.: Temporal correlation between malaria and rainfall in Sri Lanka. Malar. J. 7(1), 77 (2008)CrossRefGoogle Scholar
  19. 19.
    Brooks, R.T., Hayashi, M.: Depth-area-volume and hydroperiod relationships of ephemeral (vernal) forest pools in southern New England. Wetlands 22(2), 247–255 (2002)CrossRefGoogle Scholar
  20. 20.
    Cairns, M., Roca-Feltrer, A., Garske, T., et al.: Estimating the potential public health impact of seasonal malaria chemoprevention in African children. Nat. Commun. 3, 881 (2012)CrossRefGoogle Scholar
  21. 21.
    Caminade, C., Kovats, S., Rocklov, J., et al.: Impact of climate change on global malaria distribution. Proc. Natl. Acad. Sci. 111(9), 3286–3291 (2014)CrossRefGoogle Scholar
  22. 22.
    Carter, R., Mendis, K.N.: Evolutionary and historical aspects of the burden of malaria. Clin. Microbiol. Rev. 15(4), 564–594 (2002)CrossRefGoogle Scholar
  23. 23.
    Cator, L.J., Lynch, P.A., Read, A.F., et al.: Do malaria parasites manipulate mosquitoes? Trends Parasitol. 28(11), 466–470 (2012)CrossRefGoogle Scholar
  24. 24.
    Cator, L.J., Lynch, P.A., Thomas, M.B., et al.: Alterations in mosquito behaviour by malaria parasites: potential impact on force of infection. Malar. J. 13(1), 164 (2014)CrossRefGoogle Scholar
  25. 25.
    Center for International Earth Science Information Network (CIESIN)–Columbia University: Gridded Population of the World, version 4 (GPWv4): Population Count, Revision 10. Technical report, NASA Socioeconomic Data and Applications Center (SEDAC), Palisades (2017). https://doi.org/10.7927/H4PG1PPM|. Accessed 1 February 2018Google Scholar
  26. 26.
    Chaves, L.F., Hashizume, M., Satake, A., et al.: Regime shifts and heterogeneous trends in malaria time series from Western Kenya Highlands. Parasitology 139(1), 14–25 (2012)CrossRefGoogle Scholar
  27. 27.
    Christiansen-Jucht, C., Erguler, K., Shek, C.Y., et al.: Modelling Anopheles gambiae ss population dynamics with temperature-and age-dependent survival. Int. J. Environ. Res. Public Health 12(6), 5975–6005 (2015)CrossRefGoogle Scholar
  28. 28.
    Cohen, J.M., Smith, D.L., Cotter, C., et al.: Malaria resurgence: a systematic review and assessment of its causes. Malar. J. 11(1), 122 (2012)CrossRefGoogle Scholar
  29. 29.
    Cox, F.E.: History of the discovery of the malaria parasites and their vectors. Parasit. Vectors 3(1), 5 (2010)CrossRefGoogle Scholar
  30. 30.
    Craig, M.H., Snow, R., le Sueur, D.: A climate-based distribution model of malaria transmission in sub-Saharan Africa. Parasitol. Today 15(3), 105–111 (1999)CrossRefGoogle Scholar
  31. 31.
    Crompton, P.D., Moebius, J., Portugal, S., et al.: Malaria immunity in man and mosquito: insights into unsolved mysteries of a deadly infectious disease. Annu. Rev. Immunol. 32, 157–187 (2014)CrossRefGoogle Scholar
  32. 32.
    Curtin, P.D.: Medical knowledge and urban planning in tropical Africa. Am. Hist. Rev. 90(3), 594–613 (1985)CrossRefGoogle Scholar
  33. 33.
    Depinay, J.M.O., Mbogo, C.M., Killeen, G., et al.: A simulation model of African Anopheles ecology and population dynamics for the analysis of malaria transmission. Malar. J. 3(1), 29 (2004)CrossRefGoogle Scholar
  34. 34.
    Desconnets, J.C., Taupin, J.D., Lebel, T., et al.: Hydrology of the HAPEX-Sahel central super-site: surface water drainage and aquifer recharge through the pool systems. J. Hydrol. 188, 155–178 (1997)CrossRefGoogle Scholar
  35. 35.
    Detinova, T.S., Bertram, D., et al.: Age-Grouping Methods in Diptera of Medical Importance: With Special Reference to Some Vectors of Malaria. World Health Organization, Geneva (1962)Google Scholar
  36. 36.
    Dietz, K., Molineaux, L., Thomas, A.: A malaria model tested in the African savannah. Bull. World Health Organ. 50(3–4), 347 (1974)Google Scholar
  37. 37.
    Eikenberry, S.E., Gumel, A.B.: Mathematical modeling of climate change and malaria transmission dynamics: a historical review. J. Math. Biol. 77, 857–933 (2018)MathSciNetzbMATHCrossRefGoogle Scholar
  38. 38.
    Eling, W., Hooghof, J., van de Vegte-Bolmer, M., et al.: Tropical temperatures can inhibit development of the human malaria parasite Plasmodium falciparum in the mosquito. In: Proceedings of the Section Experimental and Applied Entomology–Netherlands Entomological Society, vol. 12, pp. 151–156 (2001)Google Scholar
  39. 39.
    Ermert, V., Fink, A.H., Jones, A.E., et al.: Development of a new version of the Liverpool Malaria Model. I. Refining the parameter settings and mathematical formulation of basic processes based on a literature review. Malar. J. 10(1), 35 (2011)Google Scholar
  40. 40.
    Ermert, V., Fink, A.H., Jones, A.E., et al.: Development of a new version of the Liverpool Malaria Model. II. Calibration and validation for West Africa. Malar. J. 10(1), 62 (2011)Google Scholar
  41. 41.
    Fick, S.E., Hijmans, R.J.: WorldClim 2: new 1-km spatial resolution climate surfaces for global land areas. Int. J. Climatol. 37(12), 4302–4315 (2017)CrossRefGoogle Scholar
  42. 42.
    Filipe, J.A., Riley, E.M., Drakeley, C.J., et al.: Determination of the processes driving the acquisition of immunity to malaria using a mathematical transmission model. PLoS Comput. Biol. 3(12), e255 (2007)MathSciNetCrossRefGoogle Scholar
  43. 43.
    Garrett-Jones, C.: Prognosis for interruption of malaria transmission through assessment of the mosquito’s vectorial capacity. Nature 204(4964), 1173–1175 (1964)CrossRefGoogle Scholar
  44. 44.
    Garrett-Jones, C., Shidrawi, G.: Malaria vectorial capacity of a population of anopheles gambiae: an exercise in epidemiological entomology. Bull. World Health Organ. 40(4), 531–545 (1969)Google Scholar
  45. 45.
    Gething, P.W., Smith, D.L., Patil, A.P., et al.: Climate change and the global malaria recession. Nature 465(7296), 342–345 (2010)CrossRefGoogle Scholar
  46. 46.
    Gething, P.W., Van Boeckel, T.P., Smith, D.L., et al.: Modelling the global constraints of temperature on transmission of Plasmodium falciparum and P. vivax. Parasit. Vectors 4(1), 92 (2011)Google Scholar
  47. 47.
    Ghani, A.C., Sutherland, C.J., Riley, E.M., et al.: Loss of population levels of immunity to malaria as a result of exposure-reducing interventions: consequences for interpretation of disease trends. PLoS One 4(2), e4383 (2009)CrossRefGoogle Scholar
  48. 48.
    Griffin, J.T., Hollingsworth, T.D., Okell, L.C., et al.: Reducing Plasmodium falciparum malaria transmission in Africa: a model-based evaluation of intervention strategies. PLoS Med. 7(8), e1000324 (2010)CrossRefGoogle Scholar
  49. 49.
    Griffin, J.T., Hollingsworth, T.D., Reyburn, H., et al.: Gradual acquisition of immunity to severe malaria with increasing exposure. Proc. R. Soc. Lond. B Biol. Sci. 282(1801), 20142657 (2015)CrossRefGoogle Scholar
  50. 50.
    Gu, W., Regens, J.L., Beier, J.C., et al.: Source reduction of mosquito larval habitats has unexpected consequences on malaria transmission. Proc. Natl. Acad. Sci. 103(46), 17560–17563 (2006)CrossRefGoogle Scholar
  51. 51.
    Gupta, S., Snow, R.W., Donnelly, C., et al.: Acquired immunity and postnatal clinical protection in childhood cerebral malaria. Proc. R. Soc. Lond. B Biol. Sci. 266(1414), 33–38 (1999)CrossRefGoogle Scholar
  52. 52.
    Gupta, S., Snow, R.W., Donnelly, C.A., et al.: Immunity to non-cerebral severe malaria is acquired after one or two infections. Nat. Med. 5(3), 340–343 (1999)CrossRefGoogle Scholar
  53. 53.
    Hay, S.I., Snow, R.W.: The malaria atlas project: developing global maps of malaria risk. PLoS Med. 3(12), e473 (2006). Malaria Atlas Project (MAP). https://map.ox.ac.uk/, Accessed 18 August 2018CrossRefGoogle Scholar
  54. 54.
    Hay, S.I., Cox, J., Rogers, D.J., et al.: Climate change and the resurgence of malaria in the East African highlands. Nature 415(6874), 905–909 (2002)CrossRefGoogle Scholar
  55. 55.
    Hay, S.I., Guerra, C.A., Tatem, A.J., et al.: The global distribution and population at risk of malaria: past, present, and future. Lancet Infect. Dis. 4(6), 327–336 (2004)CrossRefGoogle Scholar
  56. 56.
    Hayashi, M., Van der Kamp, G.: Simple equations to represent the volume–area–depth relations of shallow wetlands in small topographic depressions. J. Hydrol. 237(1-2), 74–85 (2000)CrossRefGoogle Scholar
  57. 57.
    Hoshen, M.B., Morse, A.P.: A weather-driven model of malaria transmission. Malar. J. 3(1), 32 (2004)CrossRefGoogle Scholar
  58. 58.
    Jepson, W., Moutia, A., Courtois, C.: The malaria problem in Mauritius: the bionomics of Mauritian anophelines. Bull. Entomol. Res. 38(1), 177–208 (1947)CrossRefGoogle Scholar
  59. 59.
    Karuri, S.W., Snow, R.W.: Forecasting paediatric malaria admissions on the Kenya Coast using rainfall. Glob. Health Action 9(1), 29876 (2016)CrossRefGoogle Scholar
  60. 60.
    Koenraadt, C., Githeko, A., Takken, W.: The effects of rainfall and evapotranspiration on the temporal dynamics of Anopheles gambiae s.s. and Anopheles arabiensis in a Kenyan village. Acta Trop. 90(2), 141–153 (2004)CrossRefGoogle Scholar
  61. 61.
    Lardeux, F.J., Tejerina, R.H., Quispe, V., et al.: A physiological time analysis of the duration of the gonotrophic cycle of Anopheles pseudopunctipennis and its implications for malaria transmission in Bolivia. Malar. J. 7(1), 141 (2008)CrossRefGoogle Scholar
  62. 62.
    Lindsay, S., Birley, M.: Climate change and malaria transmission. Ann. Trop. Med. Parasitol. 90(5), 573–588 (1996)CrossRefGoogle Scholar
  63. 63.
    Lunde, T.M., Bayoh, M.N., Lindtjørn, B.: How malaria models relate temperature to malaria transmission. Parasit. Vectors 6(1), 20 (2013)CrossRefGoogle Scholar
  64. 64.
    Lunde, T.M., Korecha, D., Loha, E., et al.: A dynamic model of some malaria-transmitting anopheline mosquitoes of the Afrotropical region. I. Model description and sensitivity analysis. Malar. J. 12(1), 28 (2013)Google Scholar
  65. 65.
    Lysenko, A., Semashko, I.: Geography of malaria. a medico-geographic profile of an ancient disease. Itogi Nauk. Med. Geogr., 25–146 (1968)Google Scholar
  66. 66.
    Macdonald, G.: The Epidemiology and Control of Malaria. Oxford University Press, London (1957)Google Scholar
  67. 67.
    Martens, W., Niessen, L.W., Rotmans, J., et al.: Potential impact of global climate change on malaria risk. Environ. Health Perspect. 103(5), 458–464 (1995)CrossRefGoogle Scholar
  68. 68.
    Martens, P., Kovats, R., Nijhof, S., et al.: Climate change and future populations at risk of malaria. Glob. Environ. Chang. 9, S89–S107 (1999)CrossRefGoogle Scholar
  69. 69.
    Molineaux, L., Gramiccia, G., et al.: The Garki project: research on the epidemiology and control of malaria in the Sudan savanna of West Africa. Technical report, World Health Organization (WHO), Geneva (1980). http://garkiproject.nd.edu/access-garki-data.html, Accessed 25 January 2018
  70. 70.
    Mordecai, E.A., Paaijmans, K.P., Johnson, L.R., et al.: Optimal temperature for malaria transmission is dramatically lower than previously predicted. Ecol. Lett. 16(1), 22–30 (2013)CrossRefGoogle Scholar
  71. 71.
    Nájera, J.A., González-Silva, M., Alonso, P.L.: Some lessons for the future from the global malaria eradication programme (1955–1969). PLoS Med. 8(1), e1000,412 (2011)CrossRefGoogle Scholar
  72. 72.
    Nikolov, M., Bever, C.A., Upfill-Brown, A., et al.: Malaria elimination campaigns in the Lake Kariba region of Zambia: a spatial dynamical model. PLoS Comput. Biol. 12(11), e1005192 (2016)CrossRefGoogle Scholar
  73. 73.
    Okech, B.A., Gouagna, L.C., Walczak, E., et al.: The development of Plasmodium falciparum in experimentally infected Anopheles gambiae (Diptera: Culicidae) under ambient microhabitat temperature in western Kenya. Acta Trop. 92(2), 99–108 (2004)CrossRefGoogle Scholar
  74. 74.
    Okuneye, K., Gumel, A.B.: Analysis of a temperature-and rainfall-dependent model for malaria transmission dynamics. Math. Biosci. 287, 72–92 (2017)MathSciNetzbMATHCrossRefGoogle Scholar
  75. 75.
    Okuneye, K., Eikenberry, S.E., Gumel, A.B.: Weather-driven malaria transmission model with gonotrophic and sporogonic cycles. J. Biol. Dynm. 13(S1), 288–324 (2019).MathSciNetCrossRefGoogle Scholar
  76. 76.
    Paaijmans, K.P., Wandago, M.O., Githeko, A.K., et al.: Unexpected high losses of Anopheles gambiae larvae due to rainfall. PLoS One 2(11), e1146 (2007)CrossRefGoogle Scholar
  77. 77.
    Paaijmans, K.P., Heusinkveld, B.G., Jacobs, A.F.: A simplified model to predict diurnal water temperature dynamics in a shallow tropical water pool. Int. J. Biometeorol. 52(8), 797–803 (2008)CrossRefGoogle Scholar
  78. 78.
    Paaijmans, K., Jacobs, A., Takken, W., et al.: Observations and model estimates of diurnal water temperature dynamics in mosquito breeding sites in western Kenya. Hydrol. Proced. Int. J. 22(24), 4789–4801 (2008)CrossRefGoogle Scholar
  79. 79.
    Paaijmans, K.P., Read, A.F., Thomas, M.B.: Understanding the link between malaria risk and climate. Proc. Natl. Acad. Sci. 106(33), 13844–13849 (2009)CrossRefGoogle Scholar
  80. 80.
    Paaijmans, K.P., Blanford, S., Bell, A.S., et al.: Influence of climate on malaria transmission depends on daily temperature variation. Proc. Natl. Acad. Sci. 107(34), 15135–15139 (2010)CrossRefGoogle Scholar
  81. 81.
    Paaijmans, K.P., Cator, L.J., Thomas, M.B.: Temperature-dependent pre-bloodmeal period and temperature-driven asynchrony between parasite development and mosquito biting rate reduce malaria transmission intensity. PLoS One 8(1), e55777 (2013)CrossRefGoogle Scholar
  82. 82.
    Paaijmans, K.P., Heinig, R.L., Seliga, R.A., et al.: Temperature variation makes ectotherms more sensitive to climate change. Glob. Chang. Biol. 19(8), 2373–2380 (2013)CrossRefGoogle Scholar
  83. 83.
    Packard, R.M.: The Making of a Tropical Disease: A Short History of Malaria. JHU Press, Baltimore (2007)Google Scholar
  84. 84.
    Parham, P.E., Michael, E.: Modeling the effects of weather and climate change on malaria transmission. Environ. Health Perspect. 118(5), 620–626 (2010)CrossRefGoogle Scholar
  85. 85.
    Parham, P.E., Pople, D., Christiansen-Jucht, C., et al.: Modeling the role of environmental variables on the population dynamics of the malaria vector Anopheles gambiae sensu stricto. Malar. J. 11(1), 271 (2012)CrossRefGoogle Scholar
  86. 86.
    Pascual, M., Bouma, M.J.: Do rising temperatures matter? Ecology 90(4), 906–912 (2009)CrossRefGoogle Scholar
  87. 87.
    Pascual, M., Ahumada, J.A., Chaves, L.F., et al.: Malaria resurgence in the East African highlands: temperature trends revisited. Proc. Natl. Acad. Sci. 103(15), 5829–5834 (2006)CrossRefGoogle Scholar
  88. 88.
    Perkins, S.L.: Malaria’s many mates: past, present, and future of the systematics of the order haemosporida. J. Parasitol. 100(1), 11–25 (2014)CrossRefGoogle Scholar
  89. 89.
    Reiner, R.C., Perkins, T.A., Barker, C.M., et al.: A systematic review of mathematical models of mosquito-borne pathogen transmission: 1970–2010. J. R. Soc. Interface 10(81), 20120921 (2013)CrossRefGoogle Scholar
  90. 90.
    Rogers, D.J., Randolph, S.E.: The global spread of malaria in a future, warmer world. Science 289(5485), 1763–1766 (2000)CrossRefGoogle Scholar
  91. 91.
    Ryan, S.J., Ben-Horin, T., Johnson, L.R.: Malaria control and senescence: the importance of accounting for the pace and shape of aging in wild mosquitoes. Ecosphere 6(9), 1–13 (2015)CrossRefGoogle Scholar
  92. 92.
    Ryan, S.J., McNally, A., Johnson, L.R., et al.: Mapping physiological suitability limits for malaria in Africa under climate change. Vector Borne Zoonotic Dis. 15(12), 718–725 (2015)CrossRefGoogle Scholar
  93. 93.
    Scott, T.W., Takken, W.: Feeding strategies of anthropophilic mosquitoes result in increased risk of pathogen transmission. Trends Parasitol. 28(3), 114–121 (2012)CrossRefGoogle Scholar
  94. 94.
    Shlenova, M.: The speed of blood digestion in female A. maculipennis messae at stable effective temperature. Med. Parazit. Mosk. 7, 716–735 (1938)Google Scholar
  95. 95.
    Singh, P., Yadav, Y., Saraswat, S., et al.: Intricacies of using temperature of different niches for assessing impact on malaria transmission. Indian J. Med. Res. 144(1), 67–75 (2016)CrossRefGoogle Scholar
  96. 96.
    Smith, D.L., Battle, K.E., Hay, S.I., et al.: Ross, Macdonald, and a theory for the dynamics and control of mosquito-transmitted pathogens. PLoS Pathog. 8(4), e1002588 (2012)CrossRefGoogle Scholar
  97. 97.
    Stocker, T.F., Qin, D., Plattner, G., et al.: Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change (IPCC)–Summary for Policymakers. Climate Change 2013: The Physical Science Basis (2013)Google Scholar
  98. 98.
    Thomson, M.C., Mason, S.J., Phindela, T., et al.: Use of rainfall and sea surface temperature monitoring for malaria early warning in Botswana. Am. J. Trop. Med. Hyg. 73(1), 214–221 (2005)CrossRefGoogle Scholar
  99. 99.
    Thomson, M., Doblas-Reyes, F., Mason, S., et al.: Malaria early warnings based on seasonal climate forecasts from multi-model ensembles. Nature 439(7076), 576–579 (2006)CrossRefGoogle Scholar
  100. 100.
    Tompkins, A.M., Ermert, V.: A regional-scale, high resolution dynamical malaria model that accounts for population density, climate and surface hydrology. Malar. J. 12(1), 65 (2013)CrossRefGoogle Scholar
  101. 101.
    Trape, J.F., Rogier, C., Konate, L., et al.: The Dielmo project: a longitudinal study of natural malaria infection and the mechanisms of protective immunity in a community living in a holoendemic area of Senegal. Am. J. Trop. Med. Hyg. 51(2), 123–137 (1994)CrossRefGoogle Scholar
  102. 102.
    Vermeulen, S., Zougmore, R., Wollenberg, E., et al.: Climate Change, Agriculture and Food Security (CCAFS): A global partnership to link research and action for low-income agricultural producers and consumers.Curr. Opin. Environ. Sustain. 4(1), 128–133 (2012). GCM Downscaled Data Portal. http://www.ccafs-climate.org/data_spatial_downscaling/
  103. 103.
    Webb Jr, James L.A.: The Long Struggle Against Malaria in Tropical Africa. Cambridge University Press, Cambridge (2014)Google Scholar
  104. 104.
    White, M.T., Griffin, J.T., Churcher, T.S., et al.: Modelling the impact of vector control interventions on Anopheles gambiae population dynamics. Parasit. Vectors 4(1), 153 (2011)CrossRefGoogle Scholar
  105. 105.
    World Health Organization (WHO): World Malaria Report 2015. Technical report, World Health Organization (WHO), Geneva (2015). http://www.who.int/malaria/publications/world-malaria-report-2015/report/en/
  106. 106.
    Yamana, T.K., Bomblies, A., Eltahir, E.A.: Climate change unlikely to increase malaria burden in West Africa. Nat. Clim. Chang. 6(11), 1009 (2016)CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.School of Mathematical and Statistical SciencesArizona State UniversityTempeUSA

Personalised recommendations