New tools for the study of animal trypanosomiasis in the Sudan: model-building of dangerous epidemiological passage by remote sensing geographic information systems

Recent studies in a rangeland area of Burkina Faso showed that riparian tsetse flies (Glossina tachinoides and G. palpalis gambiensis) were found along the main rivers, but depending on their location, they had different hosts and were not infected by the same trypanosomoses. There were different epidemiological situations within a distance of a few kilometres, and local assessment of the trypanosome risk thus called for a global approach taking account of the environmental and human factors involved in the interfaces between hosts and vectors. Various types of information concerning entomology, parasitology, ecology, land occupation and animal production systems were fed into a Geographical Information System. High spatial resolution remote sensing tools and original modelling methods were used to detect the valley landscapes most favourable to tsetse flies, and describe land use by herds. The impact of trypanosomes appeared to depend largely on animal movements, watering practices and the degree of contact with riparian tsetse flies. Linking these types of information revealed the most dangerous sites in epidemiological terms, which in this case represented some 18% of the network initially surveyed.     

Control of tsetse flies and trypanosomiasis: Myth or reality?

The African trypanosomiasis are among Africa's most devastating diseases. The human disease, sleeping sickness, and the animal disease, nagana, are caused by trypanosomes, protozoan parasites transmitted by tsetse flies, Glossina spp. Attempts have been made to control tsetse and trypanosomiasis for over 70 years, supported by ever-increasing amounts of foreign aid. Although progress has been made in the control of sleeping sickness, this disease still persists in many countries. Nogono excludes cattle from many of the potentially most productive areas of Africa and is a major constraint on economic development. In this paper, Robert Dransfield, Brian Williams and Robert Brightwell review the control of tsetse and trypanosomiasis in the light of recent progress in our understanding of tsetse population dynamics, with special reference to the experience gained in tsetse control on a Maasai ranch at Ngurumon in the Rift Valley of Kenya, and make suggestions for the management and funding of future control programmes in relation to rural development.     

What can we hope to gain for trypanosomiasis control from molecular studies on tsetse biology ?

At times of crisis when epidemics rage and begin to take their toll on affected populations, as we have been witnessing with African trypanosomiasis in subSahara, the dichotomy of basic versus applied research deepens. While undoubtedly the treatment of thousands of infected people is the top priority, without continued research and development on the biology of disease agents and on ecological and evolutionary forces impacting these epidemics, little progress can be gained in the long run for the eventual control of these diseases. Here, we argue the need for additional research in one under-investigated area, that is the biology of the tsetse vector. Lacking are studies aimed to understand the genetic and cellular basis of tsetse interactions with trypanosomes as well as the genetic and biochemical basis of its ability to transmit these parasites. We discuss how this knowledge has the potential to contribute to the development of new vector control strategies as well as to improve the efficacy and affordability of the existing control approaches.     

An agent-based model of sleeping sickness: simulation trials of a forest focus in southern Cameroon

An agent-based model (AMB) used to simulate the spread of Human African Trypanosomiasis is presented together with the results of simulations of a focus of the disease. This model is a completely spatialized approach taking into account a series of often overlooked parameters such as human behaviour (activity-related movements), the density and mobility of the disease vectors--tsetse flies (Glossina spp.)--and the influence of other tsetse feeding hosts (livestock and wild animal populations). The agents that represent humans and tsetse flies move in a spatially structured environment managed by specialized location agents. Existing compartmental mathematical models governed by differential equations fail to incorporate the spatial dimension of the disease transmission. Furthermore, on a small scale, transmission is unrealistically represented by entities less than one. This ABM was tested with data from one village of the Bipindi sleeping sickness focus (southern Cameroon) and with obtained realistic simulations of stable transmission involving an animal reservoir. In varying different spatial configurations, we observe that the stability of spread is linked to the spatial complexity (number of heterogeneous locations). The prevalence is very sensitive to the human densities and to the number of tsetse flies initially infected in a given location. A relatively low and durable prevalence is obtained with shortening the phase I. In addition, we discuss some upgrading possibilities, in particular the linkage to a Geographical Information System (GIS). The agent-based approach offers new ways to understanding the spread of the disease and a tool to evaluate risk and test control strategies.     

Evaluating Paratransgenesis as a Potential Control Strategy for African Trypanosomiasis

Genetic-modification strategies are currently being developed to reduce the transmission of vector-borne diseases, including African trypanosomiasis. For tsetse, the vector of African trypanosomiasis, a paratransgenic strategy is being considered: this approach involves modification of the commensal symbiotic bacteria Sodalis to express trypanosome-resistance-conferring products. Modified Sodalis can then be driven into the tsetse population by cytoplasmic incompatibility (CI) from Wolbachia bacteria. To evaluate the effectiveness of this paratransgenic strategy in controlling African trypanosomiasis, we developed a three-species mathematical model of trypanosomiasis transmission among tsetse, humans, and animal reservoir hosts. Using empirical estimates of CI parameters, we found that paratransgenic tsetse have the potential to eliminate trypanosomiasis, provided that any extra mortality caused by Wolbachia colonization is low, that the paratransgene is effective at protecting against trypanosome transmission, and that the target tsetse species comprises a large majority of the tsetse population in the release location.     

Explaining the Host-Finding Behavior of Blood-Sucking Insects: Computerized Simulation of the Effects of Habitat Geometry on Tsetse Fly Movement

Background

Male and female tsetse flies feed exclusively on vertebrate blood. While doing so they can transmit the diseases of sleeping sickness in humans and nagana in domestic stock. Knowledge of the host-orientated behavior of tsetse is important in designing bait methods of sampling and controlling the flies, and in understanding the epidemiology of the diseases. For this we must explain several puzzling distinctions in the behavior of the different sexes and species of tsetse. For example, why is it that the species occupying savannahs, unlike those of riverine habitats, appear strongly responsive to odor, rely mainly on large hosts, are repelled by humans, and are often shy of alighting on baits?

Methodology/Principal Findings

A deterministic model that simulated fly mobility and host-finding success suggested that the behavioral distinctions between riverine, savannah and forest tsetse are due largely to habitat size and shape, and the extent to which dense bushes limit occupiable space within the habitats. These factors seemed effective primarily because they affect the daily displacement of tsetse, reducing it by up to ∼70%. Sex differences in behavior are explicable by females being larger and more mobile than males.

Conclusion/Significance

Habitat geometry and fly size provide a framework that can unify much of the behavior of all sexes and species of tsetse everywhere. The general expectation is that relatively immobile insects in restricted habitats tend to be less responsive to host odors and more catholic in their diet. This has profound implications for the optimization of bait technology for tsetse, mosquitoes, black flies and tabanids, and for the epidemiology of the diseases they transmit.     

Implications of Heterogeneous Biting Exposure and Animal Hosts on Trypanosomiasis brucei gambiense Transmission and Control

The gambiense form of sleeping sickness is a neglected tropical disease, which is presumed to be anthroponotic. However, the parasite persists in human populations at levels of considerable rarity and as such the existence of animal reservoirs has been posited. Clarifying the impact of animal host reservoirs on the feasibility of interrupting sleeping sickness transmission through interventions is a matter of urgency. We developed a mathematical model allowing for heterogeneous exposure of humans to tsetse, with animal populations that differed in their ability to transmit infections, to investigate the effectiveness of two established techniques, screening and treatment of at-risk populations, and vector control. Importantly, under both assumptions, an integrated approach of human screening and vector control was supported in high transmission areas. However, increasing the intensity of vector control was more likely to eliminate transmission, while increasing the intensity of human screening reduced the time to elimination. Non-human animal hosts played important, but different roles in HAT transmission, depending on whether or not they contributed as reservoirs. If they did not serve as reservoirs, sensitivity analyses suggested their attractiveness may instead function as a sink for tsetse bites. These outcomes highlight the importance of understanding the ecological and environmental context of sleeping sickness in optimizing integrated interventions, particularly for moderate and low transmission intensity settings.     

Some general aspects of the distribution and epidemiology of bovine trypanosomosis in southern Africa

Bovine trypanosomosis occurs in vast areas of southern Africa. Its epidemiology and impact on cattle production is determined largely by the level of interaction between tsetse and cattle. Four situations can be distinguished. First, areas where cattle are absent. Second, zones where cattle have been introduced in game areas but where game is still abundant and constitutes the major source of food for tsetse. Third, areas where, often because of human interference, the density of game animals is low and cattle constitute the main source of food and finally, areas where cattle occur at the edge of tsetse-infested zones. In southern Africa, the impact of the disease on cattle production varies according to the epidemiological circumstances. The disease has an epidemic character with significant impacts on production in areas where cattle have been introduced recently or along the interface between tsetse-infested game areas and tsetse-free cultivated areas. Bovine trypanosomosis has an endemic character, with little impact on production, in areas where tsetse mainly feed on cattle and where the invasion of tsetse is low. Options for the control of bovine trypanosomosis will vary according to the epidemiological circumstance. In particular, the control of tsetse with insecticide-treated cattle will only be effective when a large proportion of feeds are taken from cattle over a large area and when the invasion of tsetse can be reduced sufficiently.     

Novel strategies targeting pathogen transmission reduction in insect vectors: Tsetse-transmitted trypanosomiasis control

Insect vectors are essential for the transmission of important human diseases such as malaria, leishmaniasis, Chagas and sleeping sickness. Insects are also responsible for the transmission of agricultural diseases that affect livestock and crops. Traditionally, control of the vector populations has been an effective disease management strategy. Recently, vector control strategies have been fortified by research in insect biology and in insect–pathogen interactions as well as by the development of transgenic technologies. In addition to insect population reduction methods, disease control via selective elimination of pathogens in insects can now be explored. Here we explore the tsetse vectors of African trypanosomes and describe the application of recent knowledge gained in their symbiotic, reproductive and vectorial biology to develop novel disease control strategies.     

Tsetse-trypanosome interactions: rites of passage.

Trypanosomes that cause sleeping sickness (Trypanosoma brucei rhodesiense and T. b. gambiense) are entirely dependent on tsetse for their transmission between hosts, but the flies are not easily infected. This situation has not arisen by chance - the tsetse has evolved an efficient defence system against trypanosome invasion. In this review, Susan Welburn and Ian Maudlin chart the progress of trypanosomes through the fly and identify some of the hazards faced by both parasite and fly that affect vector competence of tsetse.     

<Emphasis Type="Italic">Ganoderma </Emphasis>diseases of perennial crops in India – an overview

The species of Ganoderma recorded from India as causing diseases of perennial crops are listed, and their host range and taxonomy discussed. Four new hosts of G. lucidum are also reported. A decline in productivity and the death of trees are the main economic impacts due to Ganoderma diseases, and the fungus is identified as a serious pathogen of cash crops, forest plantations and trees in natural forests in the country. Ganoderma diseases have been recorded on 144 hosts in India, the major pathogens being G. lucidum and G. applanatum. G. lucidum has been recorded on 91 hosts, and appears to cause the most widespread diseases. Identification has largely been made from morphological and cultural characters, and the names currently in use should therefore be treated with caution. Cultural methods of disease control are largely inefficient in minimising inoculum pressure and in reducing the disease incidence. Chemical methods in combination with soil amendments form short-term solutions for managing the disease and improving productivity. The immediate priorities for developing an efficient management system for Ganoderma diseases in India are: (1) a thorough understanding of the etiology and epidemiology of the diseases on different hosts, (2) clarifying current ambiguity in species names, (3) assessing the inter-relationships between populations of Ganoderma on different hosts and (4) developing tools for early detection of diseases in important crops.     

Application of DNA markers to identify the individual-specific hosts of tsetse feeding on cattle

Primer sets for five different ungulate loci were used to obtain individual microsatellite DNA profiles for 29 Mashona cattle from a herd in Zimbabwe. There were 3-13 alleles for each locus and, using the entire suite of five loci, each animal within the herd, including closely related individuals, could be unequivocally distinguished. Wild-caught Glossina pallidipes Austen (Diptera: Glossinidae) were fed on specific cattle and the bloodmeal was profiled 0.5-72 h after feeding. The individual specific sources of the bloodmeals, including mixe meals produced by allowing tsetse to feed on two different cattle, were reliabl identified up to 24 h after feeding. The technique was used in field studies of hos selection by G. pallidipes and G. morsitans morsitans Westwood (Diptera Glossinidae) attracted to pairs of cattle. When the pair comprised an adult and a calf, 100% of meals were from the adult. For some pairs of adult cattle, tsetse were biased significantly towards feeding on one animal, whereas for other pairs there was no such bias. In general, feeding was greater on the animal known to have lower rate of host defensive behaviour. Results suggest that relatively slight differences in the inherent defensive behaviour of cattle produce large difference in host-specific feeding rates when the hosts are adjacent. For flies attracted to pair of cattle, < 2% contained blood from both hosts. The DNA profiling technique will be useful in studying the epidemiology of vector-borne diseases of livestock.     

Tsetse blood-meal sources,endosymbionts and trypanosome-associations in the Maasai Mara National Reserve,a wildlife-human-livestock interface

African trypanosomiasis (AT) is a neglected disease of both humans and animals caused by Trypanosoma parasites, which are transmitted by obligate hematophagous tsetse flies (Glossina spp.). Knowledge on tsetse fly vertebrate hosts and the influence of tsetse endosymbionts on trypanosome presence, especially in wildlife-human-livestock interfaces, is limited. We identified tsetse species, their blood-meal sources, and correlations between endosymbionts and trypanosome presence in tsetse flies from the trypanosome-endemic Maasai Mara National Reserve (MMNR) in Kenya. Among 1167 tsetse flies (1136 Glossina pallidipes, 31 Glossina swynnertoni) collected from 10 sampling sites, 28 (2.4%) were positive by PCR for trypanosome DNA, most (17/28) being of Trypanosoma vivax species. Blood-meal analyses based on high-resolution melting analysis of vertebrate cytochrome c oxidase 1 and cytochrome b gene PCR products (n = 354) identified humans as the most common vertebrate host (37%), followed by hippopotamus (29.1%), African buffalo (26.3%), elephant (3.39%), and giraffe (0.84%). Flies positive for trypanosome DNA had fed on hippopotamus and buffalo. Tsetse flies were more likely to be positive for trypanosomes if they had the Sodalis glossinidius endosymbiont (P = 0.0002). These findings point to complex interactions of tsetse flies with trypanosomes, endosymbionts, and diverse vertebrate hosts in wildlife ecosystems such as in the MMNR, which should be considered in control programs. These interactions may contribute to the maintenance of tsetse populations and/or persistent circulation of African trypanosomes. Although the African buffalo is a key reservoir of AT, the higher proportion of hippopotamus blood-meals in flies with trypanosome DNA indicates that other wildlife species may be important in AT transmission. No trypanosomes associated with human disease were identified, but the high proportion of human blood-meals identified are indicative of human African trypanosomiasis risk. Our results add to existing data suggesting that Sodalis endosymbionts are associated with increased trypanosome presence in tsetse flies.     

The effect of starvation on the susceptibility of teneral and non-teneral tsetse flies to trypanosome infection

Transmission of vector-borne diseases depends largely on the ability of the insect vector to become infected with the parasite. In tsetse flies, newly emerged or teneral flies are considered the most likely to develop a mature, infective trypanosome infection. This was confirmed during experimental infections where laboratory-reared Glossina morsitans morsitans Westwood (Diptera: Glossinidae) were infected with Trypanosoma congolense or T. brucei brucei. The ability of mature adult tsetse flies to become infected with trypanosomes was significantly lower than that of newly emerged flies for both parasites. However, the nutritional status of the tsetse at the time of the infective bloodmeal affected its ability to acquire either a T. congolense or T. b. brucei infection. Indeed, an extreme period of starvation (3-4 days for teneral flies, 7 days for adult flies) lowers the developmental barrier for a trypanosome infection, especially at the midgut level of the tsetse fly. Adult G. m. morsitans became at least as susceptible as newly emerged flies to infection with T. congolense. Moreover, the susceptibility of adult flies, starved for 7 days, to an infection with T. b. brucei was also significantly increased, but only at the level of maturation of an established midgut infection to a salivary gland infection. The outcome of these experimental infections clearly suggests that, under natural conditions, nutritional stress in adult tsetse flies could contribute substantially to the epidemiology of tsetse-transmitted trypanosomiasis.     

Geographical Information Systems in parasitology: a review of potential applications using the example of animal trypanosomosis in West Africa

The epidemiology of vector-borne diseases is complex due to the variability in the ecology of the different actors involved, i.e. hosts, parasites and vectors. The transmission of African animal trypanosomosis in the West-African savannah region is an excellent example of this complexity: riverine tsetse flies have an heterogeneous distribution along the rivers, depending of suitable habitats, and transmit pathogenic trypanosomes were they use domestic animal as feeding hosts. Contrasting epidemiological situations may thus occur at the local scale, and a broad view of the overall environment is necessary to quantify the interfaces in time and space between hosts and vectors. Geographical Information Systems (GIS) can provide new insight into the study of such complex epidemiological processes. GIS is a powerful technology that has been used mainly in map-making, and an enormous amount of knowledge can be gained simply by geographical data projection. GIS also allows juxtaposition of different types of information, creation of new variables, testing of theories and correlation, and generating of predictive models. The purpose of the present paper is to exemplify the potential application of GIS using a recent study carried out on animal trypanosomosis in a cattle-raising area of Burkina Faso.     

Control of human toxoplasmosis

Toxoplasmosis is caused by Toxoplasma gondii, an apicomplexan parasite that is able to infect any nucleated cell in any warm-blooded animal. Toxoplasma gondii infects around 2 billion people and, whilst only a small percentage of infected people will suffer serious disease, the prevalence of the parasite makes it one of the most damaging zoonotic diseases in the world. Toxoplasmosis is a disease with multiple manifestations: it can cause a fatal encephalitis in immunosuppressed people; if first contracted during pregnancy, it can cause miscarriage or congenital defects in the neonate; and it can cause serious ocular disease, even in immunocompetent people. The disease has a complex epidemiology, being transmitted by ingestion of oocysts that are shed in the faeces of definitive feline hosts and contaminate water, soil and crops, or by consumption of intracellular cysts in undercooked meat from intermediate hosts. In this review we examine current and future approaches to control toxoplasmosis, which encompass a variety of measures that target different components of the life cycle of T. gondii. These include: education programs about the parasite and avoidance of contact with infectious stages; biosecurity and sanitation to ensure food and water safety; chemo- and immunotherapeutics to control active infections and disease; prophylactic options to prevent acquisition of infection by livestock and cyst formation in meat; and vaccines to prevent shedding of oocysts by definitive feline hosts.     

Optimal Strategies for Controlling Riverine Tsetse Flies Using Targets: A Modelling Study

BackgroundTsetse flies occur in much of sub-Saharan Africa where they transmit the trypanosomes that cause the diseases of sleeping sickness in humans and nagana in livestock. One of the most economical and effective methods of tsetse control is the use of insecticide-treated screens, called targets, that simulate hosts. Targets have been ~1m², but recently it was shown that those tsetse that occupy riverine situations, and which are the main vectors of sleeping sickness, respond well to targets only ~0.06m². The cheapness of these tiny targets suggests the need to reconsider what intensity and duration of target deployments comprise the most cost-effective strategy in various riverine habitats.Conclusion/SignificanceSeasonal use of tiny targets deserves field trials. The ability to recognise habitat that contains tsetse populations which are not self-sustaining could improve the planning of all methods of tsetse control, against any species, in riverine, savannah or forest situations. Criteria to assist such recognition are suggested.     

Is there safety in numbers? The effect of cattle herding on biting risk from tsetse flies

In sub-Saharan Africa, tsetse (Glossina spp.) transmit species of Trypanosoma which threaten 45-50 million cattle with trypanosomiasis. These livestock are subject to various herding practices which may affect biting rates on individual cattle and hence the probability of infection. In Zimbabwe, studies were made of the effect of herd size and composition on individual biting rates by capturing tsetse as they approached and departed from groups of one to 12 cattle. Flies were captured using a ring of electrocuting nets and bloodmeals were analysed using DNA markers to identify which individual cattle were bitten. Increasing the size of a herd from one to 12 adults increased the mean number of tsetse visiting the herd four-fold and the mean feeding probability from 54% to 71%; the increased probability with larger herds was probably a result of fewer flies per host, which, in turn, reduced the hosts' defensive behaviour. For adults and juveniles in groups of four to eight cattle, > 89% of bloodmeals were from the adults, even when these comprised just 13% of the herd. For groups comprising two oxen, four cows/heifers and two calves, a grouping that reflects the typical composition of communal herds in Zimbabwe, approximately 80% of bloodmeals were from the oxen. Simple models of entomological inoculation rates suggest that cattle herding practices may reduce individual trypanosomiasis risk by up to 90%. These results have several epidemiological and practical implications. First, the gregarious nature of hosts needs to be considered in estimating entomological inoculation rates. Secondly, heterogeneities in biting rates on different cattle may help to explain why disease prevalence is frequently lower in younger/smaller cattle. Thirdly, the cost and effectiveness of tsetse control using insecticide-treated cattle may be improved by treating older/larger hosts within a herd. In general, the patterns observed with tsetse appear to apply to other genera of cattle-feeding Diptera (Stomoxys, Anopheles, Tabanidae) and thus may be important for the development of strategies for controlling other diseases affecting livestock.     

Farmer perceptions and willingness to pay for novel livestock pest control technologies: A case of tsetse repellent collar in Kwale County in Kenya

Tsetse-transmitted Animal African Trypanosomosis (AAT) is one of the most important constraints to livestock development in Africa. Use of trypanocides has been the most widespread approach for the management of AAT, despite the associated drug resistance and health concerns associated with drug metabolites in animal products. Alternative control measures that target tsetse fly vectors of AAT, though effective, have been hard to sustain in part because these are public goods applied area-wide. The International Centre of Insect Physiology and Ecology (icipe) and partners have developed and implemented a novel tsetse repellent collar (TRC) applied on animals to limit contact of tsetse flies and livestock, thereby reducing AAT transmission. The TRC has now advanced to commercialization. A household-level survey involving 632 cattle keeping households, was conducted in Shimba Hills region of Kwale County, where field trials of the TRC have been previously conducted to assess farmers’ knowledge, perception, and practices towards the management of tsetse flies, their willingness to pay (WTP) for the TRC, and factors affecting the WTP. Almost all the respondents (90%) reported that tsetse flies were the leading cattle infesting pests in the area. About 22% of these correctly identified at least four AAT clinical signs, and even though many (68%) used trypanocidal drugs to manage the disease, 50% did not perceive the drug as being effective in AAT management (50%). Few respondents (8%) were aware of the harmful effects of trypanocidal drugs. About 89% of the respondents were aware of icipe TRC, and 30% of them were using the field trial collars during the survey. Sixty-three (63%) of them were willing to pay for the TRC at the same cost they spend treating an animal for AAT. On average farmers were willing to pay KES 3,352 per animal per year. Male educated household heads are likely to pay more for the TRC. Moreover, perceived high AAT prevalence and severity further increases the WTP. Wider dissemination and commercialization of the herd-level tsetse control approach (TRC) should be encouraged to impede AAT transmission and thus enhance food security and farm incomes among the affected rural communities. Besides the uptake of TRC can be enhanced through training, especially among women farmers.     

Land cover and tsetse fly distributions in sub-Saharan Africa

Abstract.  This study aims to provide trypanosomiasis-affected countries with standardized datasets and methodologies for mapping the habitat of the tsetse fly ( Glossina spp., the disease vector) by customizing and integrating state-of-the-art land cover maps on different spatial scales. Using a combination of inductive and deductive approaches, land cover and fly distribution maps are analysed in a geographic information system (GIS) to estimate the suitability of different land cover units for the three groups (subgenera) of Glossina. All land cover datasets used for and produced by the study comply with the Land Cover Classification System (LCCS). At the continental scale, a strong correlation between land cover and tsetse habitat is found for both the fusca and palpalis groups, whereas a weaker correlation found for the morsitans group may be indicative of less restrictive ecological requirements. At the regional and national levels, thematic aggregation of the multi-purpose Africover datasets yielded high-resolution, standardized land cover maps tailored for tsetse habitat for eight East African countries. The national maps provide remarkable spatial resolution, thematic detail and geographical coverage. They may be applied in subsequent phases of tsetse and trypanosomiasis control projects, including the planning of entomological surveys, actual tsetse control operations and planning for land use in reclaimed areas. The methodology and datasets discussed in the paper may have applications beyond the tsetse and trypanosomiasis issue and may be used with reference to other arthropod vectors, vector-borne and parasitic diseases.