Distribution and Density of Tsetse Flies (Glossinidae: Diptera) at the Game/People/Livestock Interface of the Nkhotakota Game Reserve Human Sleeping Sickness Focus in Malawi

In large parts sub-Saharan Africa, tsetse flies, the vectors of African human or animal trypanosomiasis, are, or will in the foreseeable future, be confined to protected areas such as game or national parks. Challenge of people and livestock is likely to occur at the game/livestock/people interface of such infested areas. Since tsetse control in protected areas is difficult, management of trypanosomiasis in people and/or livestock requires a good understanding of tsetse population dynamics along such interfaces. The Nkhotakota Game Reserve, an important focus of human trypanosomiasis in Malawi, is a tsetse-infested protected area surrounded by a virtually tsetse-free zone. The abundance of tsetse (Glossina morsitans morsitans) along the interface, within and outside the game reserve, was monitored over 15 months using epsilon traps. A land cover map described the vegetation surrounding the traps. Few flies were captured outside the reserve. Inside, the abundance of tsetse at the interface was low but increased away from the boundary. This uneven distribution of tsetse inside the reserve is attributed to the uneven distribution of wildlife, the main host of tsetse, being concentrated deeper inside the reserve. Challenge of people and livestock at the interface is thus expected to be low, and cases of trypanosomiasis are likely due to people and/or livestock entering the reserve. Effective control of trypanosomiasis in people and livestock could be achieved by increasing the awareness among people of dangers associated with entering the reserve.     

Comparative epidemiology and control of trypanosomes

Tsetse-transmitted trypanosomiasis in man and domestic livestock is a major constraint to livestock and socio-economic development in Africa. Analysis of the limited number of databases on matching animal health and productivity available for cattle in tsetse-infested areas of Africa has provided new information about the value of current methods of controlling the disease. It was established that the trypanotolerant breeds of cattle, namely N'Dama and West African Shorthorn, were much more productive than originally believed, despite their small stature, and, as a result, could be considered for livestock development programmes in tsetse-infested regions. Moreover, in areas of low tsetse challenge, it was shown that the strategic use of therapeutic trypanocidal drugs allowed the maintenance of high levels of productivity in dairy cattle and demonstrated genotype and acquired differences in treatment requirements. On the other hand, the use of a prophylactic drug regime allowed beef cattle to be reared to an economically acceptable level of productivity in an area where tsetse challenge was high that animals rapidly succumbed if left untreated. These results show that the current methods available for the control of animal African trypanosomiasis can be effective if properly applied.     

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.     

Control of Glossina longipennis (Diptera: Glossinidae) by insecticide-treated targets at Galana ranch, Kenya, and confirmation of the role of G. longipennis as a vector of cattle trypanosomiasis

Glossina longipennis Corti was studied in Galana Ranch, Kenya over a four year period, in two areas (Tank E and Lali) where the species was abundant and other species were absent or scarce. There was active transmission of trypanosomiasis to cattle in both areas, the parasite species being Trypanosoma vivax Ziemann and T. congolense Broden. Mean infection rates of the G. longipennis were 1.1% and 0. 55% for T. vivax and T. congolense respectively at Tank E, and 0.88% and 0.15% at Lali. Experimental transmission studies showed that cattle in fly-proof enclosures challenged with wild G. longipennis collected from Galana became infected with both trypanosome species. A tsetse control operation in one area (Tank E) using targets impregnated with deltamethrin in an oil formulation reduced the population of G. longipennis by 98% over one year, despite evidence of re-invasion. Populations of G. longipennis in the other area (Lali) were relatively stable over the whole study period. The effect of tsetse control on the incidence of cattle trypanosomiasis at Tank E was less clear than that on tsetse numbers, probably due to the lack of a sustained reduction in tsetse numbers. However, a significant relationship was demonstrated between fortnightly incidence measurements and electric net catches of G. longipennis at Tank E. A further significant predictor of incidence was rainfall in the previous four to seven weeks. This study confirms the importance of G. longipennis as a vector of bovine trypanosomiasis in areas where it is the predominant tsetse present.     

Variation of tsetse fly abundance in relation to habitat and host presence in the Maasai Steppe,Tanzania

Human activities modify ecosystem structure and function and can also alter the vital rates of vectors and thus the risk of infection with vector‐borne diseases. In the Maasai Steppe ecosystem of northern Tanzania, local communities depend on livestock and suitable pasture that is shared with wildlife, which can increase tsetse abundance and the risk of trypanosomiasis. We monitored the monthly tsetse fly abundance adjacent to Tarangire National Park in 2014–2015 using geo‐referenced, baited epsilon traps. We examined the effect of habitat types and vegetation greenness (NDVI) on the relative abundance of tsetse fly species. Host availability (livestock and wildlife) was also recorded within 100×100 m of each trap site. The highest tsetse abundance was found in the ecotone between Acacia‐Commiphora woodland and grassland, and the lowest in riverine woodland. Glossina swynnertoni was the most abundant species (68%) trapped throughout the entire study, while G. pallidipes was the least common (4%). Relative species abundance was negatively associated with NDVI, with greatest abundance observed in the dry season. The relationship with the abundance of wildlife and livestock was more complex, as we found positive and negative associations depending on the host and fly species. While habitat is important for tsetse distribution, hosts also play a critical role in affecting fly abundance and, potentially, trypanosomiasis risk.     

Trypanosomiasis in Kinshasa: distribution of the vector, Glossina fuscipes quanzensis, and risk of transmission in the peri-urban area

Abstract. Because human and animal cases of African trypanosomiasis have been reported in and around the city of Kinshasa for a long time, the likelihood of local transmission was examined. A georeferenced image of the city was produced, based on a satellite image (SPOT 4). Urban, peri-urban and rural areas were delineated. All recent data on captures of Glossina fuscipes quanzensis Pires (Diptera: Glossinidae) between 1999 and 2004, as well as epidemiological data on a 1999 outbreak of human trypanosomiasis by Trypanosoma brucei gambiense in the Kisenso District, were entered in a geographical information system (GIS). Tsetse flies were mainly found along some of the major rivers in the rural and peri-urban area of Kinshasa. Unsupervised classification of the satellite image allowed identification of riverine habitats suitable for tsetse flies and indicated sites where further entomological surveys were needed. The study produced strong indications that local transmission of human trypanosomiasis had occurred in the recent past in the peri-urban zone of Kinshasa.     

Towards a rational policy for dealing with tsetse

The past 20 years have seen the development of bait technologies that enable livestock keepers to control tsetse flies and, hence, African trypanosomiasis. The techniques have, however, often been applied on too small a scale, without due regard to the realities of tsetse population dynamics. The consequent lack of progress has led to calls for a return to large-scale operations. Analysis of successful programmes to control or eliminate tsetse in southern Africa suggests that the combined use of recently improved bait methods and insecticide spraying will provide the building blocks for achieving the wider objective of the African Union, which is to create large tsetse-free zones.     

People,Patches, and Parasites: The Case of Trypanosomiasis in Zimbabwe

Understanding the socio-ecology of disease requires careful attention to the role of patches within disease landscapes. Such patches, and the interfaces between different socio-epidemiological systems, we argue, have important implications for disease control. We conducted an interdisciplinary study over three years to investigate the spatial dynamics of human and animal trypanosomiasis in the Zambezi valley, Zimbabwe. We used a habitat niche model to identify changes in suitable habitat for tsetse fly vectors over time, and this is related to local villagers’ understandings of where flies are found. Fly trapping and blood DNA analysis of livestock highlighted the patchy distribution of both flies and trypanosome parasites. Through livelihoods analysis we explored who makes use of what areas of the landscape and when, identifying the social groups most at risk. We conclude with a discussion of the practical implications, including the need for an integrated ‘One Health’ approach involving targeted approaches to both vector control and surveillance.     

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.     

Evaluation of insecticide-treated cattle as a barrier to re-invasion of tsetse to cleared areas in northeastern Zimbabwe

A field trial in Zimbabwe investigated the efficacy of insecticide-treated cattle as a barrier to prevent the re-invasion of tsetse, Glossina morsitans and G. pallidipes (Diptera: Glossinidae), into cleared areas. The original tsetse barrier consisted of insecticide-treated odour-baited targets, at an operational density of four to five targets per km2, supported by insecticide-treatments of cattle with either deltamethrin dip (Decatix, Coopers) at two-weekly intervals, or deltamethrin pouron (Spoton, Coopers) at monthly intervals, in a band approximately 20 km wide from the re-invasion front. Tsetse catch, and trypanosomiasis incidence in nine sentinel herds was recorded for 7-8 months, respectively, before the targets were removed, leaving only the insecticide treatment of the local cattle to stem the re-invasion of tsetse. After the removal of the target barrier, the tsetse readily invaded the trial area and the incidence of trypanosomiasis in sentinel herds increased, while their PCVs decreased. After seven months without the targets in place, trypanosomiasis prevalence in the local stock had reached alarmingly high levels; the trial was terminated prematurely and the target barrier re-deployed. Immediately after the re-deployment of the target barrier, the tsetse catch in the trial area reverted to acceptable levels along the re-invasion front, and trypanosomiasis incidence in the sentinel cattle decreased. It is concluded that, under the conditions of the field trial, the insecticidal treatment of local cattle did not in itself form an effective barrier to tsetse re-invasion. By contrast, the target barrier performed as was predicted by mathematical and experimental analysis, and readily cleared the tsetse infestation and reduced trypanosomosis incidence in the trial area.     

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.     

Aiming to eliminate tsetse from Africa

The problem of tsetse-transmitted trypanosomiasis occurs only in sub-Saharan Africa, where it represents a major constraint to socio-economic development. The East African form of sleeping sickness, caused by Trypanosoma brucei rhodensiense, is an acute and fatal disease, whereas the West African form, caused by Trypanosoma brucei gambiense, is generally more chronic and debilitating. The African governments have developed a new initiative, known as the Pan African Tsetse and Trypanosomiasis Eradication Campaign, which seeks to employ an area-wide approach and appropriate fly suppression methods to eradicate tsetse from areas of tsetse infestation, at a time, to ultimately create tsetse-free zones.     

A contribution towards simplifying area-wide tsetse surveys using medium resolution meteorological satellite data

A raster or grid-based Geographic Information System with data on tsetse, trypanosomiasis, animal production, agriculture and land use has recently been developed in Togo. The area-wide sampling of tsetse fly, aided by satellite imagery, is the subject of two separate papers. This paper follows on a first paper, published in this journal, describing the generation of digital tsetse distribution and abundance maps and how these accord with the local climatic and agro-ecological setting. Such maps when combined with data on the disease, the hosts and their owners, should contribute to the knowledge of the spatial epidemiology of trypanosomiasis and assist planning of integrated control operations. Here we address the problem of generating tsetse distribution and abundance maps from remotely sensed data, using a restricted amount of field data. Different discriminant analysis models have been applied using contemporary tsetse data and remotely sensed, low resolution data acquired from the National Oceanographic and Atmospheric Administration (NOAA) and Meteosat platforms. The results confirm the potential of satellite data application and multivariate analysis for the prediction of the tsetse distribution and abundance. This opens up new avenues because satellite predictions and field data may be combined to strengthen and/or substitute one another. The analysis shows how the strategic incorporation of satellite imagery may minimize field collection of data. Field surveys may be modified and conducted in two stages, first concentrating on the expected fly distribution limits and thereafter on fly abundance. The study also shows that when applying satellite data, care should be taken in selecting the optimal number of predictor variables because this number varies with the amount of training data for predicting abundance and on the homogeneity of the distribution limits for predicting fly presence. Finally, it is suggested that in addition to the use of contemporary training data and predictor variables, training and predicted data sets should refer to the same eco-geographic zone.     

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.     

The decline of a Glossina morsitans submorsitans belt in the Egbe area of the derived savanna zone, Kwara State, Nigeria

In the the early 1970s the Egbe area of Nigeria was known to be one of high trypanosomiasis risk, with four Glossina species G. morsitans submorsitans Newstead, G.longipalpis Wiedemann, G.palpalis palpalis Robineau-Desvoidy and G.tachinoides Westwood present. Grazing by Fulani pastoralists used to be short-term and only in the dry season. In recent years these pastoralists have grazed their cattle in the area throughout the year and this has prompted a reappraisal of the tsetse situation. Tsetse populations were sampled for 3 years using hand-net catches from man or an ox and biconical traps. Resident livestock, slaughter cattle and some of the flies were examined for trypanosome infection. Of the four tsetse species previously reported from the area, only the riverine species, G.p.palpalis and G.tachinoides, were encountered during the investigation. None of the 152 G.p.palpalis and 52 G.tachinoides examined was infected with trypanosomes. No infection was detected in 101 slaughtered cattle, 65 live Muturu, twelve goats and two pigs by wet film examination. However, a 14.3% Trypanosoma vivax infection rate was detected by Haematocrit Centrifugation Technique (HCT) examination in twenty-one slaughtered cattle. Increased human activities over the years had destroyed much of the vegetation and depleted the wild-life population to an extent that resulted in the disappearance of G.m.submorsitans and G.longipalpis, resulting in turn in a greatly reduced trypanosomiasis risk. It is likely that a similar trend is occurring in other areas of the Derived Savanna and Forest zones of West Africa as the human population expands.(ABSTRACT TRUNCATED AT 250 WORDS)     

Insecticide-treated cattle for tsetse control: the power and the problems

Trypanosomiasis control increasingly involves financial input from livestock owners and their active participation. If control is carried out on smaller scales than in the past, methods such as aerial and ground spraying and sterile insect techniques will have reduced application. There will be increased reliance on trypanocidal drugs, and bait methods of tsetse control--where flies are attracted to point sources and killed. If drug resistance develops, cheap and simple bait methods offer the only means of disease control that might be applied, and paid for, by stockowners themselves. The methods have been effective in some circumstances, but not in others, and it is important to understand the reasons for the successes and the failures. Analysis is presented of the results of two Tanzanian tsetse control campaigns involving the use of insecticide-treated cattle. Between 1991 and 1996, following the introduction of widespread dipping in the Kagera Region, trypanosomiasis declined from >19000 cases to <2400 and deaths from >4000 to 29. On four ranches in the region, tsetse have been almost eliminated and trypanosomiasis prophylaxis is no longer used. Similarly aggressive use of pyrethroids on Mkwaja Ranch in Tanga Region has not had such dramatic effects. Tsetse and trypanosomiasis are still common, despite high levels of prophylaxis and the deployment of approximately 200 odour-baited targets. The difference in the results is attributed to a combination of the much smaller area covered by treated animals at Mkwaja, a greater susceptibility to re-invasion and a more suitable habitat for the flies. A better understanding of the dynamics of the use of insecticide-treated cattle is needed before we can predict confidently the outcome of particular control operations.     

Insecticide-treated cattle against tsetse (Diptera: Glossinidae): what governs success?

The distributions of insecticide-treated cattle from sites in Tanzania and Zimbabwe were assessed from interviews with livestock owners, analysis of secondary livestock data and mapping technologies. The time-course of tsetse control operations at these sites were then simulated using a mathematical model that assumed diffusive movement and logistic growth in fly populations. A simulation of a tsetse control operation in Mudzi district, north-east Zimbabwe, was in accord with observations that the use of insecticide-treated cattle was unable to prevent substantial re-invasion of tsetse from Mozambique, consequent on the patchy distribution of cattle. The simulation was also consistent with the observed efficacy of a 10-km wide barrier of insecticide-treated targets deployed evenly at 4 km/(-2). Simulation of a control operation on Mkwaja Ranch in Tanzania was in accord with the observation that the use of insecticide-treated cattle reduced the tsetse population on the ranch by c. 90%. Insecticide-treated cattle were used to better effect in the Kagera Region of Tanzania. Simulation of this operation predicts that the deployment of 35,000 treated cattle in the area would result in > 99% control of the tsetse population, consistent with the observed decline, by 1-2 orders of magnitude, in cases of trypanosomiasis in the region. The greater success of the Kagera operation was due to the size and shape of the treated area and, particularly, to the restriction of re-invasion to 20% of the perimeter, compared with > 80% on Mkwaja. Simulation was used to assess how tsetse control could have been improved at Mkwaja. The results suggest that splitting herds into smaller, more numerous, units could have achieved some improvement but, in general, the disease problem would not have been solved by the use of insecticide-treated cattle alone. Only by deploying odour-baited targets in ungrazed areas, or in a 1-3-km barrier around the ranch, could substantially better control (99-99.9%) have been achieved. Sensitivity analyses of the Mkwaja simulation showed that the general conclusions were robust to assumptions regarding cattle distribution and the rates of fly movement and growth. Properly managed and appropriately applied insecticide-treated baits are powerful weapons for tsetse control but should not be used without regard to potential levels of re-invasion, consequent largely on considerations of the size and shape of the treatment area and the density and distribution of the baits.     

Identification of Glossina palpalis gambiensis specific salivary antigens: towards the development of a serologic biomarker of human exposure to tsetse flies in West Africa

The saliva of blood sucking arthropods contains a number of pharmacologically active compounds that induce an antibody response in exposed human individuals. The objectives of the present study were (i) to assess the human IgG response directed against salivary antigens of Glossina palpalis gambiensis, the main vector of Trypanosoma brucei gambiense in West Africa, as a biomarker of human–tsetse contacts; and (ii) to identify specific salivary antigens. Immune reactivity of human plasma collected within active human African trypanosomiasis (HAT) foci (coastal Guinea), historical foci where tsetse flies are still present (South-West Burkina Faso) and a tsetse free area (Bobo-Dioulasso, Burkina Faso), was measured by ELISA against whole saliva extracts. In the active HAT foci and areas where tsetse flies were present in high densities, specific IgG responses were significantly higher (p < 0.0001) to those in Bobo-Dioulasso or in Loropeni, where tsetse flies were either absent or only present at low densities. Furthermore, 2D-electrophoresis combined with mass spectrometry enabled to reveal that several antigens were specifically recognized by plasma from exposed individuals. Among them, four salivary proteins were successfully identified (Ada, 5′Nuc, Ag5 and Tsgf1). These results represent a first attempt to identify Glossina salivary proteins or synthetic peptides to develop a standardized and specific biomarker of tsetse exposure in West Africa.     

Abundance and distribution of the tsetse flies, Glossina austeni and G. brevipalpis, in different habitats in South Africa

The distribution and abundance of Glossina austeni Newstead and Glossina brevipalpis Newstead (Diptera: Glossinidae) were studied in the three main vegetation types in Zululand, KwaZulu-Natal, South Africa. During a period of 12 months, a trap transect consisting of 38 H-traps traversing the three vegetation types was monitored. The Index of Apparent Abundance (IAA) for G. brevipalpis was high in indigenous forest and open grassland but lower in exotic plantations. Glossina austeni, on the other hand, was captured mainly in or adjacent to indigenous forest. The seasonal trend in the IAA did not differ between vegetation types. The findings on the distribution of G. brevipalpis are in contrast with the historic records. Historically, this species was considered to be restricted to areas with a dense overhead canopy and high relative humidity. The repercussions of these findings for the epidemiology of livestock trypanosomiasis and the control of tsetse in Zululand are discussed.     

Artificial Warthog Burrows Used to Sample Adult and Immature Tsetse (Glossina spp) in the Zambezi Valley of Zimbabwe

BackgroundThe biology of adult tsetse (Glossina spp), vectors of trypanosomiasis in Africa, has been extensively studied – but little is known about larviposition in the field.Conclusions/SignificanceArtificial warthog burrows provide a novel method for collecting tsetse pupae, studying tsetse behaviour at larviposition, assessing the physiological status of female tsetse and their larvae, and of improving understanding of the physiological dynamics of terminal pregnancy, and population dynamics generally, with a view to improving methods of trypanosomiasis control.