Hydrology of malaria: Model development and application to a Sahelian village

[1] We present a coupled hydrology and entomology model for the mechanistic simulation of local-scale response of malaria transmission to hydrological and climatological determinants in semiarid, desert fringe environments. The model is applied to the Sahel village of Banizoumbou, Niger, to predict interannual variability in malaria vector mosquito populations that lead to variations in malaria transmission. Using a highresolution, small-scale distributed hydrology model that incorporates remotely sensed data for land cover and topography, we simulate the formation and persistence of the pools constituting the primary breeding habitat of Anopheles gambiae s.l. mosquitoes, the principal regional malaria vector mosquitoes. An agent-based mosquito population model is coupled to the distributed hydrology model, with aquatic-stage and adult-stage components. Through a dependence of aquatic-stage mosquito development and adult emergence on pool persistence, we model small-scale hydrology as a dominant control of mosquito abundance. For each individual adult mosquito, the model tracks attributes relevant to population dynamics and malaria transmission, which are updated as mosquitoes interact with their environment, humans, and animals. Weekly field observations were made in 2005 and 2006. A 16% increase in rainfall between the two years was accompanied by a 132% increase in mosquito abundance between 2005 and 2006. The model reproduces mosquito population variability at seasonal and interannual timescales and highlights individual pool persistence as a dominant control. Future developments of the presented model can be used in the evaluation of impacts of climate change on malaria, as well as the a priori evaluation of environmental management-based interventions.

[1]  Thomas A. Smith,et al.  The rise and fall of Anopheles arabiensis (Diptera: Culicidae) in a Tanzanian village. , 1995 .

[2]  W. Martens,et al.  Health impacts of climate change and ozone depletion: an ecoepidemiologic modeling approach. , 1998, Environmental health perspectives.

[3]  Andrew P. Morse,et al.  Malaria early warnings based on seasonal climate forecasts from multi-model ensembles , 2006, Nature.

[4]  W. Horsfall.  Some Responses of the Malaria Mosquito to Light , 1943 .

[5]  E. Walker,et al.  Distribution, description, and local knowledge of larval habitats of Anopheles gambiae s.l. in a village in western Kenya. , 2006, The American journal of tropical medicine and hygiene.

[6]  Antoine Flahault,et al.  The unexpected importance of mosquito oviposition behaviour for malaria: non-productive larval habitats can be sources for malaria transmission , 2005, Malaria Journal.

[7]  R. Sutherst,et al.  Global Change and Human Vulnerability to Vector-Borne Diseases , 2004, Clinical Microbiology Reviews.

[8]  Baxter E. Vieux,et al.  Hydrologic process simulation of a semiarid, endoreic catchment in Sahelian West Niger. 1. Model-aided data analysis and screening , 2003 .

[9]  John B. Silver,et al.  Mosquito Ecology: Field Sampling Methods , 2008 .

[10]  M. Gillies.,et al.  OBSERVATIONS ON THE DETERMINATION OF THE AGE COMPOSITION AND EPIDEMIOLOGICAL IMPORTANCE OF POPULATIONS OF ANOPHELES GAMBIAE GILES AND ANOPHELES FUNESTUS GILES IN TANGANYIKA. , 1964, Bulletin of the World Health Organization.

[11]  R. Novak,et al.  Host choice and multiple blood feeding behaviour of malaria vectors and other anophelines in Mwea rice scheme, Kenya , 2008, Malaria Journal.

[12]  Andrew P. Morse,et al.  A weather-driven model of malaria transmission , 2004, Malaria Journal.

[13]  C. Valentin,et al.  Land surface conditions of the Niamey region: ecological and hydrological implications , 1997 .

[14]  G. Yan,et al.  Influence of host and larval habitat distribution on the abundance of African malaria vectors in western Kenya. , 2002, The American journal of tropical medicine and hygiene.

[15]  R. Snow,et al.  A climate-based distribution model of malaria transmission in sub-Saharan Africa. , 1999, Parasitology today.

[16]  M. Coluzzi,et al.  Chromosomal differentiation and adaptation to human environments in the Anopheles gambiae complex. , 1979, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[17]  M. Copland,et al.  Activation of Anopheles gambiae mosquitoes by carbon dioxide and human breath , 1995, Medical and veterinary entomology.

[18]  G. White.  Anopheles gambiae complex and disease transmission in Africa. , 1974, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[19]  G. Gibson,et al.  Mosquito responses to carbon dioxide in B West African Sudan savanna village , 1996, Medical and veterinary entomology.

[20]  A. Kiszewski,et al.  A review of the clinical and epidemiologic burdens of epidemic malaria. , 2004, The American journal of tropical medicine and hygiene.

[21]  Christian Valentin,et al.  A runoff capability classification system based on surface features criteria in semi-arid areas of West Africa , 1992 .

[22]  G. Yan,et al.  Habitat characteristics of Anopheles gambiae s.s. larvae in a Kenyan highland , 2004, Medical and veterinary entomology.

[23]  C. Costantini,et al.  Zoophily of Anopheles arabiensis and An. gambiae in Madagascar demonstrated by odour‐baited entry traps , 2001, Medical and veterinary entomology.

[24]  J. Patz,et al.  Predicting key malaria transmission factors, biting and entomological inoculation rates, using modelled soil moisture in Kenya , 1998, Tropical medicine & international health : TM & IH.

[25]  M. Gillies.,et al.  The Anophelinae of Africa South of the Sahara , 1968 .

[26]  G. Macdonald,et al.  The analysis of infection rates in diseases in which superinfection occurs. , 1950, Tropical diseases bulletin.

[27]  Marnik Vanclooster,et al.  A global multilevel coordinate search procedure for estimating the unsaturated soil hydraulic properties , 2002 .

[28]  S. Loewenberg.  Niger welcomes largest bednet distribution in history , 2006, The Lancet.

[29]  Louis Levis.  Epidemiology and control , 2002 .

[30]  A. Haddow.  Studies of the Biting-habits of African Mosquitos. An Appraisal of Methods employed, with special Reference to the twenty-four-hour Catch , 1954 .

[31]  M. Talbot.  Environmental responses to climatic change in the West African Sahel over the past 20,000 years. , 1980 .

[32]  W. F. Jepson,et al.  The malaria problem in Mauritius; the bionomics of Mauritian anophelines. , 1947, Bulletin of entomological research.

[33]  T. Lebel,et al.  Hydrology of the HAPEX-Sahel Central Super-Site: surface water drainage and aquifer recharge through the pool systems , 1997 .

[34]  A. Clements.  The physiology of mosquitoes , 1963 .

[35]  A. M. Wasantha Lal,et al.  Performance Comparison of Overland Flow Algorithms , 1998 .

[36]  S. Lal,et al.  Epidemiology and control of malaria , 1999, Indian journal of pediatrics.

[37]  A. Torre,et al.  Density, survival and dispersal of Anopheles gambiae complex mosquitoes in a West African Sudan savanna village , 1996, Medical and veterinary entomology.

[38]  J. Bowden,et al.  The influence of moonlight on catches of insects in light-traps in Africa. Part II. The effect of moon phase on light-trap catches , 1973 .

[39]  S. Hoffman,et al.  Malaria transmission dynamics at a site in northern Ghana proposed for testing malaria vaccines , 2004, Tropical medicine & international health : TM & IH.

[40]  François Delclaux,et al.  A GIS for hydrological modelling in the semi-arid, HAPEX-Sahel experiment area of Niger, Africa , 1996, Trans. GIS.

[41]  G. Gibson,et al.  Odor-mediated host preferences of West African mosquitoes, with particular reference to malaria vectors. , 1998, The American journal of tropical medicine and hygiene.

[42]  B. Knols,et al.  Influence of Sugar Availability and Indoor Microclimate on Survival of Anopheles gambiae (Diptera: Culicidae) Under Semifield Conditions in Western Kenya , 2003, Journal of medical entomology.

[43]  R. Pollack,et al.  Enhancement of development of larval Anopheles arabiensis by proximity to flowering maize (Zea mays) in turbid water and when crowded. , 2003, The American journal of tropical medicine and hygiene.

[44]  Thierry Toutin,et al.  State-of-the-art of elevation extraction from satellite SAR data , 2000 .

[45]  Gaylon S. Campbell,et al.  Soil physics with BASIC , 1985 .

[46]  T. Lebel,et al.  Estimating hydraulic conductivity of crusted soils using disc infiltrometers and minitensiometers , 1997 .

[47]  John Russell Martin,et al.  Recommended guide for the prediction of the dispersion of airborne effluents , 1979 .

[48]  S. T. Buckland,et al.  An Introduction to the Bootstrap. , 1994 .

[49]  S. Lindsay,et al.  A malaria control trial using insecticide-treated bed nets and targeted chemoprophylaxis in a rural area of The Gambia, west Africa. 7. Impact of permethrin-impregnated bed nets on malaria vectors. , 1993, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[50]  Thierry Lebel,et al.  Rainfall climatology of the HAPEX-Sahel region during the years 1950–1990 , 1997 .

[51]  F. Sauer,et al.  Methane and carbon dioxide emissions from dairy cows in full lactation monitored over a six-month period. , 1995, Journal of dairy science.

[52]  L. Stroosnijder,et al.  Crust formation on sandy soils in the Sahel I. Rainfall and infiltration , 1984 .

[53]  D. Norris,et al.  Gene flow among populations of the malaria vector, Anopheles gambiae, in Mali, West Africa. , 2001, Genetics.

[54]  M. Cane,et al.  Using a Dynamic Hydrology Model To Predict Mosquito Abundances in Flood and Swamp Water , 2002, Emerging infectious diseases.

[55]  Mercedes Pascual,et al.  Seasonal Patterns of Infectious Diseases , 2005, PLoS medicine.

[56]  M. Thomson,et al.  Impact of Climate Variability on Infectious Disease in West Africa , 2004, EcoHealth.

[57]  J. Botella de Maglia,et al.  [Prevention of malaria]. , 1999, Revista clinica espanola.

[58]  Leduca,et al.  Long-term rise in a Sahelian water-table : the Continental Terminal in South-West Niger , 2002 .

[59]  M. Gillies.,et al.  The Role of Carbon Dioxide in Host-Finding by Mosquitoes (Diptera: Culicidae): A Review , 1980 .

[60]  L. F. Chaves,et al.  Malaria resurgence in the East African highlands: temperature trends revisited. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[61]  S W Lindsay,et al.  Temperature‐related duration of aquatic stages of the Afrotropical malaria vector mosquito Anopheles gambiae in the laboratory , 2004, Medical and veterinary entomology.

[62]  Weltgesundheitsorganisation.  World malaria report , 2005 .

[63]  M. Gillies..  Studies on the dispersion and survival of Anopheles gambiae Giles in East Africa, by means of marking and release experiments , 1961 .

[64]  T S DETINOVA,et al.  Age-grouping methods in Diptera of medical importance with special reference to some vectors of malaria. , 1962, Monograph series. World Health Organization.

[65]  David Pollard,et al.  Use of a land-surface-transfer scheme (LSX) in a global climate model: the response to doubling stomatal resistance , 1995 .

[66]  J. Beier,et al.  Spatial distribution and habitat characterization of anopheline mosquito larvae in Western Kenya. , 1999, The American journal of tropical medicine and hygiene.

[67]  W. Takken,et al.  Odor-mediated behavior of Afrotropical malaria mosquitoes. , 1999, Annual review of entomology.

[68]  T. Lebel,et al.  Typology of Rainfall Fields to Improve Rainfall Estimation in the Sahel by the Area Threshold Method , 1996 .

[69]  John C. Carlson,et al.  A simulation model of African Anopheles ecology and population dynamics for the analysis of malaria transmission , 2004, Malaria Journal.

[70]  G. Yan,et al.  Relationships Between Occurrence of Anopheles gambiae s.l. (Diptera: Culicidae) and Size and Stability of Larval Habitats , 2005, Journal of medical entomology.

[71]  Michael D Samuel,et al.  Modeling the Population Dynamics of Culex quinquefasciatus (Diptera: Culicidae), along an Elevational Gradient in Hawaii , 2004, Journal of medical entomology.

[72]  Joel Schwartz,et al.  Weather-based prediction of Plasmodium falciparum malaria in epidemic-prone regions of Ethiopia II. Weather-based prediction systems perform comparably to early detection systems in identifying times for interventions , 2004, Malaria Journal.

[73]  C. Curtis.  Mosquito ecology: field sampling methods (2nd edn): edited by M.W Service, Elsevier Applied Science, 1992. £200.00 (xiii + 998 pages) ISBN 1 85166 798 9 , 1993 .

[74]  W. Takken,et al.  Cannibalism and predation among larvae of the Anopheles gambiae complex , 2003, Medical and veterinary entomology.

[75]  H. D. Pratt.  Influence of the moon on light trap collections of Anopheles albimanus in Puerto Rico. , 1948, Journal. National Malaria Society.