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.     

Genetics and trypanotolerance

Genetic resistance to disease and its use in domestic livestock usually ranks last, if at all, amongst preferred disease control measures - usually preceded by measures such as chemotherapy, vector control and vaccination. Thus, interest in genetic resistance is often a reflection of dissatisfaction with other control strategies, and the current emphasis on trypanotolerant cattle in Africa is just such a case. Eighty years of tsetse fly eradication programmes have had little impact on tsetse distribution, although recent research with odour baited targets impregnated with insecticide brings hope for the future. The search for a vaccine has proved more arduous than anticipated and the number of drugs available for therapy and prophylaxis is limited. In the search for alternative solutions to the problem of African trypanosomiasis, attention has recently focused on genetic resistance - a subject normally covered by immunologists or veterinarians(3-7). In this article, Rosemary Dolan discusses the concept from the geneticist's viewpoint.     

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.     

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.     

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.     

Population vulnerability and disability in Kenya's tsetse fly habitats

Background

Human African Trypanosomiasis (HAT), also referred to as sleeping sickness, and African Animal Trypanosomaisis (AAT), known as nagana, are highly prevalent parasitic vector-borne diseases in sub-Saharan Africa. Humans acquire trypanosomiasis following the bite of a tsetse fly infected with the protozoa Trypanosoma brucei (T.b.) spp. –i.e., T.b. gambiense in West and Central Africa and T.b. rhodesiense in East and Southern Africa. Over the last decade HAT diagnostic capacity to estimate HAT prevalence has improved in active case-finding areas but enhanced passive surveillance programs are still lacking in much of rural sub-Saharan Africa.

Methodology/Principal Findings

This retrospective-cross-sectional study examined the use of national census data (1999) to estimate population vulnerability and disability in Kenya''s 7 tsetse belts to assess the potential of HAT-acquired infection in those areas. A multilevel study design estimated the likelihood of disability in individuals, nested within households, nested within tsetse fly habitats of varying levels of poverty. Residents and recent migrants of working age were studied. Tsetse fly''s impact on disability was conceptualised via two exposure pathways: directly from the bite of a pathogenic tsetse fly resulting in HAT infection or indirectly, as the potential for AAT takes land out of agricultural production and diseased livestock leads to livestock morbidity and mortality, contributing to nutritional deficiencies and poverty. Tsetse belts that were significantly associated with increased disability prevalence were identified and the direct and indirect exposure pathways were evaluated.

Conclusions/Significance

Incorporating reports on disability from the national census is a promising surveillance tool that may enhance future HAT surveillance programs in sub-Saharan Africa. The combined burdens of HAT and AAT and the opportunity costs of agricultural production in AAT areas are likely contributors to disability within tsetse-infested areas. Future research will assess changes in the spatial relationships between high tsetse infestation and human disability following the release of the Kenya 2009 census at the local level.     

The prevalence of African animal trypanosomoses and tsetse presence in Western Senegal

In 2005, the Government of Senegal initiated a tsetse eradication campaign in the Niayes and La Petite C?te aiming at the removal of African Animal Trypanosomosis (AAT), which is one of the main constraints to the development of more effective cattle production systems. The target area has particular meteorological and ecological characteristics that provide great potential for animal production, but it is unfortunately still infested by the riverine tsetse species Glossina palpalis gambiensis Vanderplank (Diptera: Glossinidae). The tsetse project in Senegal has adopted an area-wide integrated pest management (AW-IPM) approach that targets the entire tsetse population within a delimited area. During the first phase of the programme, a feasibility study was conducted that included the collection of entomological, veterinary, population genetics, environmental and socioeconomic baseline data. This paper presents the parasitological and serological prevalence data of AAT in cattle residing inside and outside the tsetse-infested areas of the target zone prior to the control effort. At the herd level, a mean parasitological prevalence of 2.4% was observed, whereas a serological prevalence of 28.7%, 4.4%, and 0.3% was obtained for Trypanosoma vivax, T. congolense and T. brucei brucei, respectively. The observed infection risk was 3 times higher for T. congolense and T. vivax in the tsetse-infested than in the assumed tsetse-free areas. Moreover, AAT prevalence decreased significantly with distance from the nearest tsetse captured which indicated that cyclical transmission of the parasites by tsetse was predominant over mechanical transmission by numerous other biting flies present. The importance of these results for the development of a control strategy for the planned AW-IPM campaign is discussed.     

How do African game animals control trypanosome infections?

African trypanosomiasis is endemic over much of sub-saharan Africa. But whereas domestic animals - especially cattle - often succumb to the infection, wild mammals generally show a high degree o f resistance. Many species o f wildlife living in tsetse-infested areas carry trypanosome infections, and so act as important reservoir hosts, but generally show no obvious ill-effects. How they survive the infection is an important question in understanding mechanisms o f trypanotolerance, yet relevant data are sparse and scattered. Here, Ayub Mulla and Roy Rickman review some of the previous studies to illustrate how complex the question is.     

Repurposing the orphan drug nitisinone to control the transmission of African trypanosomiasis

Tsetse transmit African trypanosomiasis, which is a disease fatal to both humans and animals. A vaccine to protect against this disease does not exist so transmission control relies on eliminating tsetse populations. Although neurotoxic insecticides are the gold standard for insect control, they negatively impact the environment and reduce populations of insect pollinator species. Here we present a promising, environment-friendly alternative to current insecticides that targets the insect tyrosine metabolism pathway. A bloodmeal contains high levels of tyrosine, which is toxic to haematophagous insects if it is not degraded and eliminated. RNA interference (RNAi) of either the first two enzymes in the tyrosine degradation pathway (tyrosine aminotransferase (TAT) and 4-hydroxyphenylpyruvate dioxygenase (HPPD)) was lethal to tsetse. Furthermore, nitisinone (NTBC), an FDA-approved tyrosine catabolism inhibitor, killed tsetse regardless if the drug was orally or topically applied. However, oral administration of NTBC to bumblebees did not affect their survival. Using a novel mathematical model, we show that NTBC could reduce the transmission of African trypanosomiasis in sub-Saharan Africa, thus accelerating current disease elimination programmes.

This study shows that tsetse flies, vectors of African trypanosomiasis, are highly susceptible to killing by nitisinone, a tyrosine catabolism inhibitor currently used to treat human metabolic diseases; this environment-friendly drug could facilitate elimination of African trypanosomiasis and other diseases transmitted by blood feeding insects.     

Geographic Information Systems and the Selection of Priority Areas for Control of Tsetse-transmitted Trypanosomiasis in Africa

In this paper, Tim Robinson describes the use of geographic information systems (GIS) to prioritize areas for tsetse and trypanosomiasis control in Zambia. Digital maps of land tenure, percentage agriculture, stocking rates and relative arable potential are combined within a GIS to identify areas where trypanosomiasis is a direct constraint to agricultural development and where the presence of tsetse prevents access to areas adjacent to those under high pressure from livestock and agriculture. The techniques described in this paper could be applied to a range of livestock diseases in many parts of the world.     

Options for vector control against trypanosomiasis in Africa

Tsetse control has long been an important option for reducing the impact of African trypanosomiasis but, although many effective methods have been used, the results have seldom proved sustainable. Developments to reduce cost and environmental impact increasingly limit the choices available for control and the scale of operations has declined. Conversely, human trypanosomiasis has reached epidemic proportions in some countries. Here, Reg Allsopp argues that those tasked with managing trypanosomiasis or committed to poverty alleviation in Africa should consider large-scale, area-wide tsetse control involving all proven methods, including aerial spraying and the sterile insect technique.     

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.     

Trypanosomiasis and Tsetse Control with Insecticidal Pour-ons- Fact and Fiction?

Insecticidal pour-ons that are applied directly to cattle have been promoted widely in the last decade as a new means of controlling tsetse flies in Africa. Tsetse attracted to treated cattle get a lethal dose of insecticide and die. Following a large trial in Kenya, Matthew Baylis and Peter Stevenson argue here that the reduction in trypanosomiasis incidence caused by pour-ons exceeds that expected from the impact (if there is any) on the tsetse population and that certain other (as yet unknown) factors must also be involved.     

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.     

Admixture and diversity in West African cattle populations

We present a population genetic analysis of microsatellite variation in 16 West African cattle populations. West Africa represents a unique juxtaposition of different climatic and ecological zones in a relatively small geographical area. While more humid coastal regions are inhabited by the tsetse fly, a vector which spreads trypanosomiasis among cattle, the disease is not transmitted in the drier areas outside this zone. This is the most thorough study of genetic diversity in cattle within this area, which contains genetically important trypanotolerant Bos taurus breeds. Genetic relationships among the many breeds are examined and levels of diversity are assessed. Admixture levels were determined using a variety of methods. Ancestry informative or population-associated alleles (PAAs) were selected using populations from India, the Near East and Europe. Multivariate analysis, the admix program and model-based Bayesian admixture analysis approaches were also employed. These analyses reveal the direct impact of ecological factors and the profound effect of admixture on the cattle of this region. They also highlight the importance of efforts to prevent further dilution of African taurine breeds by B. indicus cattle.     

Immunological approaches to the control of animal trypanosomiasis

Control of African trypanosomiasis relies heavily on attempts to eliminate the tsetse fly vectors, and the use of trypanocidal drugs which are not entirely satisfactory. But the prospects for immunological control have a long history - since the last century, explorers and settlers in Africa have progressively exposed their horses and cattle to tsetse bites (a process known as 'salting') in an attempt to build up some degree of immunity to the disease. More recently, immunologists and biochemists have used modern techniques to explore the possibility of suitable vaccines. In this article, Vinand Nantuyla discusses the problems and possible contributions of the immunological approach.     

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.     

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.     

Cattle-tsetse contact in relation to the daily activity patterns of Glossina morsitans submorsitans in The Gambia

Abstract. The daily flight activity patterns of one of the main vectors of animal trypanosomiasis in West Africa, Glossina morsitans submorsitans , were assessed using four different methods. Results from all the methods showed that there was some flight activity nearly every hour in all seasons but they differed in the level of contact between grazing cattle herds and G.m.submorsitans. In the late dry season, trap data indicated that there was negligible activity from midday to late afternoon, whereas observations of tsetse contact with cattle herds or hand-net collections on herd followings showed no fall in attack rates on the cattle by G.m.submorsitans.
Differences between trap and animal-baited collection data may be attributable to the type of G.m.submorsitans sampled by each method. Male G.m.submorsitans captured by traps were more fat depleted than those caught on ox-baited flyrounds or by hand-net collections on herd followings. All methods showed that male G.m.submorsitans were most fat depleted in the late dry season and least in the early dry season. It was concluded that the traps were mainly sampling the spontaneous flights of G.m.submorsitans. Hunger and endogenous rhythms increase the likelihood of spontaneous flights towards dusk, particularly in conditions such as those at midday in the very hot, late dry season. However, the presence of cattle herds in infested habitats probably activated nearby G.m.submorsitans and the continual movement through the grazing areas ensured contact with tsetse throughout grazing.
The data indicated that strategic management of herd grazing times cannot eliminate the risk of trypanosomiasis transmission occurring, irrespective of the harshness of the dry season climate. An assessment of the level of this risk could only be measured suitably by collecting tsetse using animal-baited methods, not from trap data.     

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)