Ecology of a vector-borne zoonosis in a complex ecosystem: trypanosomiasis in Serengeti, Tanzania

Abstract

Unravelling the complexities of a disease with multiple wildlife host and multiple tsetse vector species is no easy task. After over a century of field observations, experimental studies, anecdotal evidence and conjecture, the role of wildlife in the transmission of trypanosomes is still unclear. Recently, however, frameworks used in the studies of other vector-borne diseases with wildlife reservoirs showed that not only is it possible to understand transmission, but that spatio-temporal predictions of human disease risk and targeted control are realistic aims, even in such complex systems. This thesis explores the epidemiology of human African trypanosomiasis (HAT) in the Serengeti-Mara ecosystem in Northern Tanzania, where recent cases in tourists have highlighted the disease as a public health and economic concern. Assessment of the prevalence of trypanosome infections in different wildlife species is the first step in investigating the relative importance of different species in disease transmission. Identification of trypanosomes relies on sensitive and specific diagnostic tests. Polymerase chain reaction (PCR) protocols based on interspecies differences in the length of the ribosomal internal transcribed spacer (ITS) regions have been widely used in livestock to identify multiple trypanosome species in one PCR reaction. This study represents the first assessment of these protocols on blood samples collected from wildlife. Clonal sequence analysis of PCR products revealed a large range of trypanosomes circulating in wildlife, including Trypanosoma congolense, Trypanosoma brucei, Trypanosoma simiae Tsavo, Trypanosoma godfreyi and Trypanosoma vivax. In addition sequences similar to known sequences, termed Trypanosoma simiae-like and T. vivax-like trypanosomes, may reflect further diversity. However, further characterisation is needed before ITS protocols can be used widely for epidemiological studies in wildlife. The prevalence of T. brucei s.l. and T. congolense varied widely between species. This variation was predominantly explained by taxonomic classification, suggesting intrinsic differences in response to trypanosomes. Trypanosoma brucei rhodesiense, the subspecies responsible for HAT, was identified in lion, hyaena and reedbuck. Age significantly affected the prevalence of T. congolense in lion and hyaena, with the highest prevalence in subadults. The lack of statistically significant differences in prevalence between animals sampled live or after death confirmed that post-mortem sampling provides a method for increasing sample sizes in wildlife studies. The complex relationship between tsetse density and prevalence of trypanosome infections illustrated the difficulties of assessing data from diverse ecosystems with many potential confounding factors. A cross-sectional study of Glossina swynnertoni and Glossina pallidipes, the main tsetse species in Serengeti, highlighted the difficulties of integrating the results of microscopy and PCR to generate meaningful measures of the prevalence of transmissible T. brucei infections for epidemiological studies. However, PCR results suggested that G. pallidipes may be more important as a vector of T. brucei s.l. than has been previously recognised. Spatial variation in both tsetse density and the prevalence of trypanosome infections suggests human disease risk is heterogeneous. The results of this study, along with relevant literature, are considered within the context of frameworks used for other vector-borne diseases and the implications for disease management discussed.