In the Mouhoun River basin, Burkina Faso, the main vectors of African animal trypanosomoses are Glossina palpalis gambiensis Vanderplank and Glossina tachinoides Westwood (Diptera: Glossinidae), both of which are riverine tsetse species. The aim of our study was to understand the impact of landscape anthropogenic changes on the seasonal dynamics of vectors and associated trypanosomosis risk. Three sites were selected on the basis of the level of disturbance of tsetse habitats and predominant tsetse species: disturbed (Boromo, for G. tachinoides) and half-disturbed (Douroula for G. tachinoides and Kadomba for G. p. gambiensis). At each of these sites, seasonal variations in the apparent densities of tsetse and mechanical vectors and tsetse infection rates were monitored over 17 months. Tsetse densities differed significantly between sites and seasons. Of 5613 captured tsetse, 1897 were dissected; 34 of these were found to be infected with trypanosomes. The most frequent infection was Trypanosoma vivax (1.4%), followed by Trypanosoma congolense (0.3%) and Trypanosoma brucei (0.05%). The mean physiological age of 703 tsetse females was investigated to better characterize the transmission risk. Despite the environmental changes, it appeared that tsetse lived long enough to transmit trypanosomes, especially in half-disturbed landscapes. A total of 3021 other biting flies from 15 species (mainly Tabanidae and Stomoxyinae) were also caught: their densities also differed significantly among sites and seasons. Their relative importance regarding trypanosome transmission is discussed; the trypanosomosis risk in cattle was similar at all sites despite very low tsetse densities (but high mechanical vector densities) in one of them.

Spatio-temporal distribution of tsetse and other biting flies in the Mouhoun River basin, Burkina Faso

In Burkina Faso, the cyclical vectors of African animal trypanosomoses (AAT) are riverine tsetse species, namely Glossina palpalis gambiensis Vanderplank (G.p.g.) and Glossina tachinoides Westwood (G. t.) (Diptera: Glossinidae). Experimental work demonstrated that environmental stress can increase the sensitivity of tsetse to trypanosome infection. Seasonal variations of the tsetse infection rates were monitored monthly over 17 months (May 2006-Sept 2007) in two sites (Douroula and Kadomba). In total, 1,423 flies were dissected and the infection of the proboscis, middle intestine and salivary glands was noted. All the positive organs were analyzed using monospecific polymerase chain reaction (PCR) primers. To investigate the role of different environmental factors, fly infection rates were analyzed using generalized linear mixed binomial models using the species, sex, and monthly averages of the maximal, minimal and mean daily temperatures, rainfalls, Land Surface Temperature day (LSTd) and night (LSTn) as fixed effects and the trap position as a random effect. The overall infection rate was 10% from which the predominant species was T. congolense (7.6% of the flies), followed by T. vivax (2.2% of the flies). The best model (lowest AICc) for the global infection rates was the one with the maximal daily temperature only as fixed effect (p<0.001). For T. congolense, the best model was the one with the tsetse species, sex, maximal daily temperature and rainfalls as fixed effect, where the maximal daily temperature was the main effect (p<0.001). The number of T. vivax infections was too low to allow the models to converge. The maturation rate of T. congolense was very high (94%), and G. t. harbored a higher maturation rate (p=0.03). The results are discussed in view of former laboratory studies showing that temperature stress can increase the susceptibility of tsetse to trypanosomes, as well as the possibility to improve AAT risk mapping using satellite images.

/pdf/dynamics-of-tsetse-natural-infection-rates-in-the-mouhoun-3llspnghof.pdf

Dynamics of tsetse natural infection rates in the Mouhoun river, Burkina Faso, in relation with environmental factors

Trypanosomiasis has been identified as a neglected tropical disease in both humans and animals in many regions of sub-Saharan Africa. Whilst assessments of the biology of trypanosomes, vectors, vertebrate hosts and the environment have provided useful information about life cycles, transmission, and pathogenesis of the parasites that could be used for treatment and control, less information is available about the effects of interactions among multiple intrinsic factors on trypanosome presence in tsetse flies from different sites. It is known that multiple species of tsetse flies can transmit trypanosomes but differences in their vector competence has normally been studied in relation to individual factors in isolation, such as: intrinsic factors of the flies (e.g. age, sex); habitat characteristics; presence of endosymbionts (e.g. Wigglesworthia glossinidia, Sodalis glossinidius); feeding pattern; host communities that the flies feed on; and which species of trypanosomes are transmitted. The purpose of this study was to take a more integrated approach to investigate trypanosome prevalence in tsetse flies. In chapter 2, techniques were optimised for using the Polymerase Chain Reaction (PCR) to identify species of trypanosomes (Trypanosoma vivax, T. congolense, T. brucei, T. simiae, and T. godfreyi) present in four species of tsetse flies (Glossina austeni, G. brevipalpis, G. longipennis and G. pallidipes) from two regions of eastern Kenya (the Shimba Hills and Nguruman). Based on universal primers targeting the internal transcribed spacer 1 region (ITS-1), T. vivax was the predominant pathogenic species detected in flies, both singly and in combination with other species of trypanosomes. Using Generalised Linear Models (GLMs) and likelihood ratio tests to choose the best-fitting models, presence of T. vivax was significantly associated with an interaction between subpopulation (a combination between collection sites and species of Glossina) and sex of the flies (X2 = 7.52, df = 21, P-value = 0.0061); prevalence in females overall was higher than in males but this was not consistent across subpopulations. Similarly, T. congolense was significantly associated only with subpopulation (X2 = 18.77, df = 1, P-value = 0.0046); prevalence was higher overall in the Shimba Hills than in Nguruman but this pattern varied by species of tsetse fly. When associations were analysed in individual species of tsetse flies, there were no consistent associations between trypanosome prevalence and any single factor (site, sex, age) and different combinations of interactions were found to be significant for each. The results thus demonstrated complex interactions between vectors and trypanosome prevalence related to both the distribution and intrinsic factors of tsetse flies. The potential influence of the presence of S. glossinidius on trypanosome presence in tsetse flies was studied in chapter 3. A high number of Sodalis positive flies was found in the Shimba Hills, while there were only two positive flies from Nguruman. Presence or absence of Sodalis was significantly associated with subpopulation while trypanosome presence showed a significant association with age (X2 = 4.65, df = 14, P-value = 0.0310) and an interaction between subpopulation and sex (X2 = 18.94, df = 10, P-value = 0.0043). However, the specific associations that were significant varied across species of trypanosomes, with T. congolense and T. brucei but not T. vivax showing significant interactions involving Sodalis. Although it has previously been concluded that presence of Sodalis increases susceptibility to trypanosomes, the results presented here suggest a more complicated relationship, which may be biased by differences in the distribution and intrinsic factors of tsetse flies, as well as which trypanosome species are considered. In chapter 4 trypanosome status was studied in relation to blood meal sources, feeding status and feeding patterns of G. pallidipes (which was the predominant fly species collected for this study) as determined by sequencing the mitochondrial cytochrome B gene using DNA extracted from abdomen samples. African buffalo and African elephants were the main sources of blood meals but antelopes, warthogs, humans, giraffes and hyenas were also identified. Feeding on multiple hosts was common in flies sampled from the Shimba Hills but most flies from Nguruman had fed on single host species. Based on Multiple Correspondence Analysis (MCA), host-feeding patterns showed a correlation with site of sample collection and Sodalis status, while trypanosome status was correlated with sex and age of the flies, suggesting that recent host-feeding patterns from blood meal analysis cannot predict trypanosome status. In conclusion, the complexity of interactions found suggests that strategies of tsetse fly control should be specific to particular epidemic areas. Future studies should include laboratory experiments that use local colonies of tsetse flies, local strains of trypanosomes and local S. glossinidius under controlled environmental conditions to tease out the factors that affect vector competence and the relative influence of external environmental factors on the dynamics of these interactions.

Prevalence and associations of Trypanosoma spp. and Sodalis glossinidius with intrinsic factors of tsetse flies

SUMMARY Efficient, cyclical transmission of trypanosomes through tsetse flies is central to maintenance of human sleeping sickness and nagana across sub-Saharan Africa. Infection rates in tsetse are normally very low as most parasites ingested with the fly bloodmeal die in the fly gut, displaying the characteristics of apoptotic cells. Here we show that a range of antioxidants (glutathione, cysteine, N-acetyl-cysteine, ascorbic acid and uric acid), when added to the insect bloodmeal, can dramatically inhibit cell death of Trypanosoma brucei brucei in tsetse. Both L- and D-cysteine invoked similar effects suggesting that inhibition of trypanosome death is not dependent on protein synthesis. The present work suggests that antioxidants reduce the midgut environment protecting trypanosomes from cell death induced by reactive oxygen species.

Antioxidants promote establishment of trypanosome infections in tsetse.: Antioxidants promote establishment of trypanosome infections in tsetse.

Abstract African Animal Trypanosomosis (AAT) is a parasitic disease caused by trypanosome species, posing a major challenge to animal health and production in Africa. In the Matutuíne District, southern Mozambique, where Glossina brevipalpis is prevalent, AAT is endemic. Previous research conducted in South Africa suggested that G . brevipalpis plays a marginal role in the transmission of Trypanosoma congolense . However, considering the wide distribution of G. brevipalpis in Southeast Africa and the major epidemiological implications of the aforementioned observations, this study was designed to re-assess the vectorial competence of G. brevipalpis in the transmission of T. congolense- savannah type. The research involved 915 G. brevipalpis flies, fed six times on two cattle infected with T. congolense . After 48 hours, the flies were later fed on a non-infected animal to clean the proboscis, followed by extended feeding on four susceptible cattle for 22 days. These five clean animals were monitored for 60 days based on body temperature, packed cell volume, buffy coat technique and polymerase chain reaction. In the meantime, flies were dissected weekly to observe the development of trypanosomes in the midgut and proboscis. To discard any possible mechanical transmission by G. brevipalpis 48 hours after an infected blood meal, 97 flies from a colony were fed once on two infected cattle and once on a susceptible bovine. The Spearman correlation and Mann-Whitney U tests were used to analyse the data. Results showed that the four susceptible cattle became infected with T. congolense , while the animal used for proboscis cleaning and discard any mechanical transmission remained uninfected. Dissections revealed that 89% of flies were positive for trypanosome through microscopy and 100% through PCR. These findings confirm that G. brevipalpis is a competent biological vector for transmitting T. congolense, challenging earlier assumptions and emphasizing its role in AAT dynamics. 

Evaluation of the vectorial competence of Glossina brevipalpis in the transmission of Trypanosoma congolense-savannah type, in the Matutuíne District, Maputo Province, Mozambique

The obligate blood feeding tsetse fly (Diptera: Glossinidae) is an essential component in the cyclical transmission of several African trypanosome species such as Trypanosoma congolense and T. brucei spp., causing devastating diseases in both human and animal in sub-Saharan Africa. The proportion of trypanosome-infected tsetse is a major determinant of the transmission dynamics of the disease and is affected by various endogenous and exogenous factors. Recently, the nutritional state of the flies at the time of their infective bloodmeal was demonstrated to affect the susceptibility of teneral and older flies to infections with T. congolense or T. b. brucei. The experimental work that is presented in this thesis aimed i) to determine whether nutritional stress affects the ability of tsetse flies to develop human pathogenic trypanosome species, ii) to explore the underlying mechanism that induce an increased susceptibility in starved tsetse flies with focus on the tsetse fly’s immunological abilities and finally iii) to determine the effects of seasonal climatic changes on the nutritional status and immune peptide expression in field-caught tsetse flies in order to determine whether changes in environmental conditions affect the trypanosome transmission dynamics in the field.

/pdf/effect-of-nutritional-stress-on-the-tsetse-fly-s-vector-kn3f6vpz3l.pdf

Effect of nutritional stress on the tsetse fly’s vector competence and its implications on trypanosome transmission in the field

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Effect of nutritional stress on the tsetse fly’s vector competence and its implications on trypanosome transmission in the field