Modelling ecological and socioeconomic feedbacks of Buruli ulcer in sub-Saharan Africa: results from a field study in Cameroon

Abstract

BackgroundBuruli ulcer, caused by Mycobacterium ulcerans, is an emerging and devastating skin disease associated with a great morbidity and disability burden in tropical regions. Emergence and geographical distribution of Buruli ulcer have been consistently associated with anthropogenic changes to aquatic ecosystems, but the ecology, transmission, and economic effects of the disease in endemic populations are still poorly described. The challenges faced for Buruli ulcer are representative of a wider group of sapronoses and neglected diseases whose complex ecological dynamics undermine our efforts to quantify the health impacts of environmental change. We aimed to characterise key factors driving the ecology, method of transmission, and effect of Mycobacterium ulcerans on human populations. MethodsWe combined an extensive longitudinal environmental field survey in two endemic areas of Cameroon with (1) generalised linear mixed models to understand factors associated with M ulcerans environmental dynamics, (2) fitting of deterministic mathematical models to study Buruli ulcer transmission, and (3) theoretical simulations in agent-based models to characterise economic impacts of Buruli ulcer in endemic areas. FindingsWe show how the ecological dynamics of M ulcerans are the result of a complex interaction between abiotic and biotic factors in freshwater ecosystems. We found positive significant associations of M ulcerans presence with seasonal climatic factors and physicochemical characteristics in stagnant waters. We observed a different association with the abundance and diversity of aquatic organisms depending on water conditions, notably pH. We provide the first field evidence that the predominant transmission route from the aquatic ecosystem to human populations might be through direct inoculation of the bacteria into the skin in contaminated environments, contrary to the vector-borne transmission postulated in the past decade. Median force of infection in the set of model simulations that best fitted the data was more than 200 times higher for proxies of direct environmental transmission than for vector-borne transmission. Based on these results, we show theoretically that in contexts of high environmental risk, Buruli ulcer can cause economic inequalities at the population level, with disproportionate effects on the poorest socioeconomic groups due to disparities in vulnerability and health-care access. While average loss of per capita wealth at equilibrium due to Buruli ulcer was less than 10% at the highest environmental risk, the poorest 10% lost up to 40% of their wealth, resulting in measurable increases in the population's Theil Index. InterpretationThe negative consequences of land-use change could fall disproportionally on the poor through disease-mediated feedbacks. These novel results reveal the urgent need to extend such inter-disciplinary approaches (ie, at the interface of disease ecology, human epidemiology and economic development) to better quantify anthropogenic impacts on environmentally-persistent diseases and inform appropriate control strategies in low-resource settings. FundingFrench National Research Agency, French School of Public Health, and Young International Research Teams of AIRD/IRD.