Research Article: Ecological Drivers of Mansonella perstans Infection in Uganda and Patterns of Co-endemicity with Lymphatic Filariasis and Malaria

Date Published: January 21, 2016

Publisher: Public Library of Science

Author(s): Anna-Sofie Stensgaard, Penelope Vounatsou, Ambrose W. Onapa, Jürg Utzinger, Erling M. Pedersen, Thomas K. Kristensen, Paul E. Simonsen, Patrick J. Lammie.

Abstract: BackgroundMansonella perstans is a widespread, but relatively unknown human filarial parasite transmitted by Culicoides biting midges. Although it is found in many parts of sub-Saharan Africa, only few studies have been carried out to deepen the understanding of its ecology, epidemiology, and health consequences. Hence, knowledge about ecological drivers of the vector and parasite distribution, integral to develop spatially explicit models for disease prevention, control, and elimination strategies, is limited.MethodologyWe analyzed data from a comprehensive nationwide survey of M. perstans infection conducted in 76 schools across Uganda in 2000–2003, to identify environmental drivers. A suite of Bayesian geostatistical regression models was fitted, and the best fitting model based on the deviance information criterion was utilized to predict M. perstans infection risk for all of Uganda. Additionally, we investigated co-infection rates and co-distribution with Wuchereria bancrofti and Plasmodium spp. infections observed at the same survey by mapping geographically overlapping areas.Principal FindingsSeveral bioclimatic factors were significantly associated with M. perstans infection levels. A spatial Bayesian regression model showed the best fit, with diurnal temperature range, normalized difference vegetation index, and cattle densities identified as significant covariates. This model was employed to predict M. perstans infection risk at non-sampled locations. The level of co-infection with W. bancrofti was low (0.3%), due to limited geographic overlap. However, where the two infections did overlap geographically, a positive association was found.Conclusions/SignificanceThis study presents the first geostatistical risk map for M. perstans in Uganda. We confirmed a widespread distribution of M. perstans, and identified important potential drivers of risk. The results provide new insight about the ecologic preferences of this otherwise poorly known filarial parasite and its Culicoides vector species in Uganda, which might be relevant for other settings in sub-Saharan Africa.

Partial Text: The human filarial parasite Mansonella perstans has been considered as one of the most prevalent human parasites in Africa [1]. Despite the wide distribution, only very few studies have addressed its epidemiology and associated health consequences, and currently no effective drug therapy for treatment, control, and local elimination is available [2]. Indeed, M. perstans is viewed as one of the most neglected of the neglected tropical diseases (NTDs) [2].

The present study provided countrywide, model-based prevalence maps for M. perstans in Uganda, at a high spatial resolution. To our knowledge this is the first study to apply rigorous Bayesian geostatistical risk mapping to national survey data of this neglected human parasitic infection. The study furthermore identified risk factors and displayed high prevalence areas, and thus provides new insights into the ecological preferences of the unknown vector (Culicoides spp.). The resulting maps were finally combined with geostatistical risk maps previously developed for bancroftian filariasis and malaria [9], to delineate overlapping areas (co-distributions) and to investigate levels of co-infection and parasite-parasite associations. Overall, the investigations provide a deeper understanding of the zoogeographical patterns of this widespread, yet little studied parasitic infection, of importance for integrated disease control planning and implementation [11].



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