thesis

Field observations and mechanistic modeling of the malaria transmission response to environmental climatic variability

Abstract

Thesis (Ph. D.)--Massachusetts Institute of Technology, Dept. of Civil and Environmental Engineering, 2009.Includes bibliographical references (leaves 205-222).A coupled HYDrology, Entomology and MAlaria Transmission Simulator (HYDREMATS) has been developed. The model simulates the hydrological and climatological determinants of malaria transmission mechanistically and at high spatialand temporal resolution, and is valid for semi-arid, desert fringe environments where the mosquito Anopheles gambiae s.l. is the dominant malaria vector. This includes much of the most malarious parts of Africa such as the Sahel. The model is validated with several years of field data collected from Banizoumbou village in southwestern Niger. Simulations of the 2005 and 2006 rain seasons in Banizoumbou using measured meteorological data successfully reproduce the observed interannual variability in malaria vector mosquito abundance. The distributed hydrology model operates at high spatial and temporal resolution, and incorporates remotely-sensed data for land cover and topography to simulate the formation and persistence of the small, temporary pools that constitute the breeding habitat of Anopheles gambiae s.l. mosquitoes. An agent-based mosquito population model is coupled to the distributed hydrology model, with aquatic stage and adult stage components. Aquatic stage mosquitoes are allowed to breed in any surface water, but the developing eggs, larvae and pupae die if the pool dries. The model structure maintains the spatial relationships of breeding pools, mosquitoes, and human habitation. For each individual adult mosquito, the model tracks the attributes relevant to population dynamics and malaria transmission, which are updated as mosquitoes interact with their environment, humans, and animals.(cont.) The model reproduces mosquito population variability at seasonal and interannual time scales, and highlights individual pool persistence as a dominant control of mosquito population dynamics. HYDREMATS is applied to study the impact of village-scale spatial variability in hydrologic conditions on malaria transmission. Zindarou is a village located only 30 km from Banizoumbou, but hydrologically it is very different from Banizoumbou. The groundwater table around Banizoumbou is about 25 meters below the surface, while the groundwater table around Zindarou is a few meters below the surface. HYDREMATS reproduces the much higher mosquito populations observed in Zindarou arising from the lush, wet conditions compared to drier Banizoumbou. This result exposes small scale spatial variability in surface and subsurface hydrology as a principal control of villagescale malaria transmission. Further experiments simulate the effect of climate shifts on Sahel malaria-transmitting mosquito abundance using HYDREMATS. Climate variability and climate change in West Africa often occur in the form of a shift from a wet regime to a dry regime or vice versa. Such a climate shift in the West African Sahel can greatly impact the intensity of regional malaria transmission. To investigate possible outcomes of such shifts, meteorological data from two different Sahel stations are used as alternate climatic forcings for the Banizoumbou model domain. The stations are located north and south of Banizoumbou in Agoufou, Mali, and in Djougou, Benin at 200 km and 400 km in the north-south direction from Banizoumbou, respectively.(cont.) These data series represent possible climate shift scenarios, based on the observation that a northward or southward translation of Sahelian climate conditions along the north-south gradient has accompanied past climate shifts. A series of simulations investigate individually the effects of precipitation frequency and ambient temperature on anopheles mosquito populations and vectorial capacity. The vectorial capacity with Djougou, Benin conditions exhibited a 25% increase compared to baseline Banizoumbou conditions, whereas the vectorial capacity decreased by 26% with the Agoufou, Mali meteorological conditions. Isolation of temperature contributions to these differences show that in a cooling scenario (to resemble Benin), elasticity of mosquito abundance is 1.3, compared to -8.9 for the shift to hotter conditions found in Agoufou, Mali. Mosquito mortality ultimately limits malaria transmission in shifts to warmer conditions, and parasite extrinsic incubation period (sporogony) becomes limiting at low temperatures. In all cases, changes in precipitation frequency can limit mosquito breeding due to small-scale hydrological processes influencing breeding pool persistence. Finally, a simple model of human immune response to malaria transmission is built into HYDREMATS. The HYDREMATS representation of acquired immunity acting in opposition to-yet depending on-malaria parasite in the bloodstream explains field observations of very similar malaria prevalence in Zindarou and Banizoumbou despite pronounced difference in vectorial capacity.(cont.) The results are consistent with various paradoxical observations in the literature of unexpectedly low prevalence with higher biting pressure. HYDREMATS represents acquired immunity as dependent on repeated inoculations of malaria, with a slow loss of immunity in the absence of infectious bites. Because climate variability determines variability in vectorial capacity, in an endemic environment acquired immunity level in a human population has a memory of past climate variability. Model experiments in Banizoumbou evaluating the impacts of climate shifts confirm this.by Arne Bomblies.Ph.D

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