Research Article: A Theoretical Analysis of the Geography of Schistosomiasis in Burkina Faso Highlights the Roles of Human Mobility and Water Resources Development in Disease Transmission

Date Published: October 29, 2015

Publisher: Public Library of Science

Author(s): Javier Perez-Saez, Lorenzo Mari, Enrico Bertuzzo, Renato Casagrandi, Susanne H. Sokolow, Giulio A. De Leo, Theophile Mande, Natalie Ceperley, Jean-Marc Froehlich, Mariam Sou, Harouna Karambiri, Hamma Yacouba, Amadou Maiga, Marino Gatto, Andrea Rinaldo, Song Liang.

Abstract: We study the geography of schistosomiasis across Burkina Faso by means of a spatially explicit model of water-based disease dynamics. The model quantitatively addresses the geographic stratification of disease burden in a novel framework by explicitly accounting for drivers and controls of the disease, including spatial information on the distributions of population and infrastructure, jointly with a general description of human mobility and climatic/ecological drivers. Spatial patterns of disease are analysed by the extraction and the mapping of suitable eigenvectors of the Jacobian matrix subsuming the stability of the disease-free equilibrium. The relevance of the work lies in the novel mapping of disease burden, a byproduct of the parametrization induced by regional upscaling, by model-guided field validations and in the predictive scenarios allowed by exploiting the range of possible parameters and processes. Human mobility is found to be a primary control at regional scales both for pathogen invasion success and the overall distribution of disease burden. The effects of water resources development highlighted by systematic reviews are accounted for by the average distances of human settlements from water bodies that are habitats for the parasite’s intermediate host. Our results confirm the empirical findings about the role of water resources development on disease spread into regions previously nearly disease-free also by inspection of empirical prevalence patterns. We conclude that while the model still needs refinements based on field and epidemiological evidence, the proposed framework provides a powerful tool for large-scale public health planning and schistosomiasis management.

Partial Text: National programs for schistosomiasis control and elimination require appraising spatial patterns of endemic disease under variable conditions accounting for changing epidemiological drivers and controls inclusive of varying exposure rates, human mobility, habitat ranges for the intermediate host and the complexities of the parasite’s life cycle. Patterns of waterborne disease are unique in their spatial complexity which arise from pathogen reproduction, transport and transmission through waterways and human mobility networks, and for the corresponding challenges to morbidity and transmission control. Indeed both micro- and macro-parasitic waterborne diseases are conditioned by spatially varying natural (environmental or climatic [1–3]) and anthropogenic factors (water resources, [4–6] habitat availability and suitability [7], pathogen dispersal by river networks [8–11], and human mobility [12–16]. Here we focus on the transmission cycle of schistosomiasis, a parasitic disease, which is emblematic of the interplay among spatially varying drivers and controls. Schistosomiasis, or bilharzia, is a chronic debilitating disease caused by parasitic worms of genus Schistosoma that affected an estimated 249 million people around the world in 2012. A crushing 93% of these people live in Sub-Saharian Africa [17], where both the urinary and intestinal forms of the disease, caused by S. haematobium and S. mansoni respectively, are present. This figure has grown from 77% in 2006 [18]. Both forms of schistosomiasis have been reported in Burkina Faso since the early fifties, with measured prevalences prior to the implementation of Mass Drug Administration Campaigns (MDAs) within the Schistosomiasis Control Initiative (SCI) [19] systematically higher than 30% [20, 21]. A North-to-South decreasing gradient was observed for the urinary form of the disease and an opposite trend for the intestinal one [21]. The MDAs had a important impact on prevalence with immediate post-MDA prevalence levels ten times lower than pre-treatment baseline, but levels of infection have in some cases risen again in recent years, with some villages back to pre-treatment conditions [22]. Challenges to the successful control of the disease are manifold due to the complexity of the transmission cycle, which requires freshwater aquatic snails (Bulinus spp. or Biomphalaria spp. for S. haematobium and S. mansoni respectively) as obligate intermediate hosts. The transmission cycle consists of the excretion of parasite eggs from human to water bodies where they hatch into miracidia, the first larval stage, which infect the aquatic snail intermediate host. Asexual reproduction therein produces second-stage larvae called cercariae which infect humans through skin penetration. Once in the human host, they migrate in the system, mature into adult schistosomes and mate in the capillary surrounding the bladder or the intestine depending on the parasite genus leading to egg production and excretion. Environmental, climatic, ecological and socio-economic factors drive the transmission cycle by conditioning both snail and human probability of infection [12]. Dynamical models of schistosomiasis [23, 24], and their spatial extension to connected environments [12], provide the opportunity to show the applicability of a general mathematical framework for analysing the disease invasion conditions and the resulting spatial patterns of human schistosomiasis which could inform control and elimination programs. With this goal, we study schistosomiasis spread and persistence in the context of Burkina Faso with an emphasis on the roles of human mobility and water resources development.



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