New approaches to the integrated control of trypanosomosis

ELSEVIER Veterinary Parasitology 71 (1997) 121-135

veterinary parasitology

New approaches to the integrated control of trypanosomosis

P . H . H o l m e s 1

University of Glasgow Veterinary. School, Bearsden Road, Glasgow G61 1QH, UK

Abstract

Trypanosomosis is one of the most devastating diseases of animals and man in Sub-Saharan Africa. Over the past century numerous methods of control have been developed yet the disease has proved very difficult to eradicate. Current methods to control the parasite, in the absence of a vaccine, have to rely on the use of trypanocidal drugs and trypanotolerant breeds of livestock. Vector control previously depended on ground and aerial spraying of insecticide but now depends on the use of traps, targets and bait technology. The application of insecticides to cattle is currently of particular interest. Unfortunately all of the current methods of control have disadvan- tages and none has proved to be sustainable. There is growing interest in integrated control which can be at three levels; integration with rural development, integration with other disease control measures and integration of various tsetse and trypanosomosis control measures.

It is anticipated that distinct benefits can be achieved by an integrated approach which will improve the effectiveness of control and enhance the prospects of sustainability. © 1997 Elsevier Science B.V.

Keywords: Trypanosomosis; Control; Tstetse fly; Sub-Saharan Africa; Trypanosoma

1. Introduction

Trypanosomosis is one of the most devastating diseases of animals and man in Sub-Saharan Africa and has a profound effect on rural development over vast areas.

It has remained the hope of many of those associated with African development that tsetse and trypanosomosis may be successfully eradicated from the continent. However the disease has proved to be difficult to control despite intensive efforts over most of this century and most attempts to achieve eradication have failed. Where eradication has

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122 P.H. Holmes/Veterinat 3, Parasitology 71 (1997) 121-135

been achieved this has been accompanied by extensive settlement and changes in land use, e.g. in Nigeria. In many other situations long lasting control has not been achieved although the problem has often been diminished for considerable periods of time by adequately funded campaigns against the vector. Unfortunately periods of successful control of tsetse flies have frequently been followed by re-invasion and many of the earlier benefits have been lost. The reasons for the failure to maintain control measures for adequate periods of time include social, economic and political factors or civil unrest and conflict. As a result re-invasion of cleared areas by tsetse from neighbouring fly belts quickly occurs.

It has been suggested that the most environmentally acceptable method currently available for eradicating tsetse should consist of an integrated campaign using insecticide treated screens or traps followed by massive releases of sterile males (Bauer et al., 1992b). Such schemes have been attempted for example in southwest Burkina Faso (Cuisance et al., 1984) and more recently in Zanzibar. In the former site re-invasion of tsetse was restricted by barriers for some years. However when external funding of the running costs for the maintenance of the barriers came to an end the whole system rapidly collapsed and re-invasion of tsetse occurred.

The history of the project in Burkina Faso is an example of the problems almost inevitably encountered, namely that tsetse campaigns fail not primarily because of technical inadequacies but because they have not been sustainable without external funding. The most serious challenge facing the future of tsetse and trypanosomosis control is how to achieve sustainability using local resources.

It is now broadly accepted that tsetse control and disease management is a more realistic goal than eradication. Furthermore in many areas farmers prefer suppression rather than eradication as a more economic option and will tolerate a low residual population of tsetse flies and the associated disease risk, which can be managed by a combination of control techniques.

2. Current methods of control and their sustainability

In the absence of an effective vaccine the control of trypanosomosis has to depend on the use of trypanocidal drugs, trypanotolerant breeds of livestock, tsetse traps and insecticides.

2.1. Chemoprophylaxis and chemotherapy

Trypanocidal drugs are the most well established and widespread method of control in most African countries (Holmes and Scott, 1982). However only three drugs are available for use against tsetse transmitted trypanosomosis, principally in cattle, and three drugs for use in camels against Trypanosoma evansi. They are diminazene, isometamidium and homidium.

With the exception of mel-cy which is used in camels, all the drugs have been on the market for over 30 years. They remain popular with farmers because they allow treatment of individual animals, they are relatively cheap and commonly available. Approximately 30 million doses are used each year. They have proved to be a

P.H. Holmes/Veterinary. Parasitology 71 (1997) 121-135 123

sustainable method of control and their positive impact has been enormous (Holmes and Torr, 1988).

The benefits of chemoprophylaxis have been quantified in a number of studies. One of the most extensive studies ever undertaken was at the Mkwaja Ranch in Tanzania (Trail et al., 1985). In this unique study an analysis was made of matching animal health, animal productivity, and trypanocidal treatment data based on more than 20 000 calving records over the 10 year period from 1973 to 1982. The ranch had approximately 12000 head of Grade Boran cattle which could not survive without the use of trypanocidal drugs. The number of treatments administered to each animal was on average 4.6 isometamidium and 0.7 diminazene aceturate treatments per year. A very high level of productivity was achieved under this drug regime which approximated to 80% of that achieved by Boran cattle reared on tsetse-free ranches in Kenya, which are considered to be some of the best in the world. The study demonstrated that in an area of Africa where cattle, if left untreated, rapidly succumbed to trypanosomosis, the strategic use of the prophylactic drug isometamidium under a high standard of management could permit cattle to survive and be productive.

Later, a study using similar production parameters to those used at Mkwaja was conducted in village cattle in a tsetse-infested area on the Kenyan coast (Itty et al., 1987). The study showed that where livestock are exposed to low-to-medium trypanosomosis risk, cattle production was more profitable when they were treated prophylacti- cally with trypanocidal drugs rather than merely receiving therapeutic treatments. On an individual herd basis, the superiority of the prophylactic drug regime was directly related to the increase in lactation yield.

Following the demise of state-funded veterinary services across Africa the use of trypanocidal drugs is increasingly unsupervised and it is suspected that under-dosage commonly occurs. This has probably contributed to the apparent increase in drug resistance, with resistance now reported from many African countries. In some cases multiple resistance against all three cattle trypanocides has been demonstrated (Per- egrine, 1994). However in most African countries the prevalence and impact of drug resistance is largely unknown and requires investigation.

There are two further threats to the future sustainable use of trypanocide drugs. First, availability, since the market is perceived to be relatively unprofitable because of the relative poverty of African farmers, there has been a reluctance by pharmaceutical companies to develop new drugs against trypanosomosis. Furthermore companies are reluctant to maintain the production of existing drugs if this requires significant investment, e.g. to address new health and safety issues or when mergers of pharmaceutical companies occur and less profitable products may be abandoned. Secondly, fake drugs are a growing international menace to both human and animal health. Recent surveys suggest that many compounds for sale in local African pharmacies have little or no therapeutic activity. It has recently been estimated that 60% of the drugs available in developing countries are fakes (Broussard, 1996).

2.2. Trypanotolerant livestock

It is well established that many breeds of ruminants display an ability to tolerate trypanosome infections at a level which kills more susceptible breeds. The N'dama

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breed of cattle of West Africa is perhaps the best described and many studies using experimental infections have demonstrated its trypanotolerance. Furthermore the genetic resistance displayed by this breed extends to other important diseases, including haemonchosis, tick burdens, and dermatophilosis (Murray et al., 1982). However the ability to tolerate these diseases is not absolute and in areas of heavy tsetse challenge trypanotolerant cattle such as the N'dama can succumb to infection. Trypanotolerant cattle and small ruminants present a method of control which is likely to be sustainable. However some factors do mitigate against this. First, their distribution is essentially limited to West Africa and secondly, even within West Africa there is the perception that, because they are relatively small in size, they are less productive and farmers prefer to move to larger breeds or increase the level of Zebu blood in their stock when the tsetse challenge is diminished by changes in land use patterns or through control programmes (Jabbar et al., 1995).

2.3. Vector control

2.3.1. Ground spraying This technique aims to apply a deposit of residual insecticide to resting sites of tsetse

on vegetation where it remains lethal to tsetse beyond the maximum pupal period of about 60 days. In the past, dieldrin and DDT have been commonly used. However, the use of residual insecticides, especially organochlorines is now environmentally and politically unacceptable. More recently pyrethroids have been applied by this method. However, there are major logistical problems with the technique, such as developing adequate access, maintaining a fleet of vehicles and spraying equipment; and planning and supervising large numbers of spray-teams. Attempts have been made to overcome these logistical problems by applying residual deposits of insecticide by helicopter.

Ground spraying is the only proven method of large-scale tsetse eradication: the technique was used to eliminate tsetse from 200000 knl 2 of Nigeria. (Jordan, 1978).

2.3.2. Aerial spraying As a result of the decline in ground spraying, aerial spraying was increasingly

adopted in the 1970s and 1980s using particularly the sequential aerosol technique. Like ground spraying, this technique aims to kill all adult flies over a single pupal period. Very low doses of insecticide are applied as aerosols either from low flying fixed-wing aircraft or from helicopters, killing tsetse by direct contact. Since the insecticide is applied at very low doses there are no residual effects. Generally five applications are made, sufficient to eliminate emerging flies over the maximum pupal period.

The technique demands skilled pilots, sophisticated navigation equipment, and care- fully controlled and monitored application. It has large logistical advantages over ground spraying as a result of reduced labour demands and the centralisation of activities and support facilities (Holmes and Torr, 1988). However it is expensive and requires substantial funding at national and international level. There is little community participation and it is rarely sustainable unless barriers against re-invasion and surveillance programmes are rigorously established and maintained, or unless an isolated flybelt is eradicated.

P.H. Holmes//Veterinary Parasitology 71 (1997) 121-135 125

2.3.3. Traps, targets and bait technology Unlike ground or aerial spraying this technique attempts to exert a modest daily

mortality of 2 -3% of the female population; the cumulative effect is a 95% reduction in the population per year in the absence of immigration.

In the early 1970s the bi-conical trap was developed and successfully used against riverine species such as G. palpalis palpalis (Allsopp, 1984). At about the same time G. Vale and his colleagues in Zimbabwe demonstrated that conventional traps failed to catch many of the tsetse that visited them and that most of the tsetse attracted to a stationary animal did so in response to the host's odour (Vale, 1980).

Carbon dioxide and acetone were found to be powerful attractants of tsetse. Bu- tanone, 1-octen-3-ol, p-cresol, 4-methylphenol and 3-n propylphenol have also been identified as attractants. The catch of a trap baited with all these components except carbon dioxide (which is too expensive and impractical to use on a large scale) is increased by as much as 20-fold for some species of tsetse. However many components of cattle odour have remained elusive, and the most effective cocktails of attractants are still less than 50% as attractive to tsetse as natural cattle odours. In order to reduce a dependency on imported chemicals, cow urine has been used with some success.

Over the past decade cheaper and simpler targets have been developed. These are insecticide-treated cloth screens baited with synthetic odours. The flies come into contact with the target and pick up a lethal dose of insecticide. The target design elicits this contact by exploiting the visual responses of tsetse. Targets are usually deployed at 4 per km 2 although a higher density is used for barriers.

Following outstanding success in selected areas of Zimbabwe the technique has been applied in several countries.

Targets have the advantage of being relatively more effective and cheaper than traps, although the latter have the distinct advantage of displaying dead tsetse flies, which helps to motivate local people to participate in schemes using this technique.

In view of the relatively low cost of the materials and unsophisticated technology, targets and traps combined with odour attractants have been advocated as the most sustainable method of tsetse control. They are particularly suitable for community-based tsetse control programmes. However there are potential and real difficulties in their implementation. The targets and traps require regular supervision to combat damage and theft, and their effectiveness varies between species and geographic subspecies of Glossina.

Difficulties have also emerged in maintaining the motivation of local communities to provide and service the targets and traps. Eventually all the control costs must be borne by the cattle-owning households in the community, and there are several problems associated with this. Much depends on the individual's willingness to contribute labour and money and this is strongly influenced by their perception of the problem, which changes with time. Those living in the centres of controlled areas may receive greater benefits yet be less willing to contribute than those living on the periphery. Cleared areas must be protected against re-invasion by the maintenance of barriers, using targets and traps. In general the greater the cleared area the greater the length of the barrier and the long term commitment required by cattle owners to maintain the barrier.

In areas with low cattle densities the costs to protect each animal will be greater and

126 P.H. Holmes/Veterina~ Parasitology 71 (1997) 121-135

it is generally more difficult to obtain sustained commitments from livestock owners in such situations.

The success of community-based target control schemes is also dependent on the continued availability of target material, including insecticide, at prices which the livestock owners can afford.

In the schemes described so far a facilitator supported by external funding has usually been involved, and the success of the scheme has depended on their presence. The sustainability of community-based tsetse control schemes using targets remains to be fully assessed.

2.3.4. Lice bait technology In recent years there has been great interest in using insecticide sprays, dips or

pour-ons for cattle in tsetse-infested areas as moving targets, which have advantages over stationary targets, in terms of maintenance and vulnerability to theft. Synthetic pyrethroids have been the chemicals of choice. The chemicals used do not have a repellent effect and their knockdown activity is more persistent than the killing effect. Nevertheless because the flies have to land repeatedly, primarily because of the defensive reactions of the animal, the uptake of insecticide may be enhanced and lead to paralysis of the flies before they can probe and feed, thereby reducing the risk of transmission of trypanosomosis (Bauer et al., 1992a). The schemes have had considerable success and major reductions in tsetse populations have been achieved. Treatment of cattle with insecticide is likely to prove the cheapest method of tsetse eradication in situations where sufficient cattle and veterinary infrastructure are present to make it practicable (Barrett, 1997). The insecticides used for this purpose also reduce the numbers of nuisance flies and ticks in the location of the treated cattle and this provides an important additional incentive to farmers to maintain treatments. The treatments must be given on a regular basis and the chemicals are relatively expensive.

In a study reported by Bauer et al. (1995) 2000 ranch cattle in Burkina Faso were treated with 1% deltamethrin in an area of high tsetse density. After four treatments at monthly intervals, the time between treatments was increased to 2 months. Eleven months after beginning the campaign the fly population, measured as f l ies / t rap/day, had decreased by 98%. The incidence of trypanosomosis fell and weight gains in calves improved.

The schemes in Burkina Faso using pour-ons have found good support from local livestock owners who are willing to pay for insecticide treatment of their cattle. There are currently plans to reduce treatment to only twice a year (B. Bauer, personal communication, 1996).

At present the limits to the technique are poorly defined and a number of factors need to be addressed before this technology can be advocated for widespread use. These factors include, the cattle densities required to ensure effective control, the scope for treating only a proportion of the cattle, and the percentage of tsetse blood meals which must be from cattle to ensure success of this technique.

The sustainability of this method of control will also depend on the cost and availability of the insecticides, farmer motivation to ensure that sufficient cattle are treated, the expected emergence of pyrethroid resistance by the ticks and nuisance/bi-

P.H. Holmes/Veterinary Parasitology 71 (1997) 121-135 127

ting flies and possible difficulties with tick-borne diseases resulting from the loss of enzootic stability when tick numbers decline.

3. Integrated control

There are three levels at which integrated control of tsetse and trypanosomosis can be addressed; integration with rural development, integration with other disease control measures (integrated disease management), and integration of various tsetse and trypanosomosis control measures.

3.1. Integration of control with rural development

In Sub-Saharan Africa, trypanosomosis and land use are closely inter-related. The disease has direct effects on the well-being of the rural population through mortality, reduced productivity of domestic livestock and the costs of control, e.g. drug treatment.

There are also substantial indirect effects of trypanosomosis largely through prevent- ing agricultural development of potentially productive land (Putt et al., 1980). This applies particularly to situations where the keeping of draught oxen is prevented by trypanosomosis, as their presence has great advantages for the farmer in determining the area which can be cultivated. In such situations expensive control schemes can only be justified if they are associated with sustainable rural development. Increased livestock and arable crop production may then be sufficient to maintain control schemes in the long-term. Tsetse control which does not lead to environmental degradation may be applied in wilderness areas to safeguard gains made in adjacent settled areas. However, local government should be sufficiently well established to ensure that random settlement and depletion of natural resources in cleared areas does not occur.

Decisions on control schemes are therefore influenced by the potential of agricultural areas and efforts should be directed primarily towards high-medium potential areas in which substantial populations of humans and livestock occur and where the disease threatens land use and/or productivity. Land use planning is essential before control activities are undertaken and must involve the participation of the affected community. However, community participation must extend beyond the planning and into implementation in order to improve the likelihood of sustainability. The prospects for sustainability will be highest in high-medium potential areas which are also the most favourable for cost recovery and involvement of the private sector, whilst the risks of environmental degradation are less than in marginal areas.

In high-medium potential agricultural areas it is likely that the influx of humans and livestock and the associated productivity will be sufficient to achieve full cost recovery using tsetse target technology. However in medium-Now potential areas, cost recovery is unlikely to be achieved using targets, and drugs will provide a better return for farmers except where resistance to trypanocidal drugs occurs.

In the past, many technically successful tsetse and trypanosomosis control schemes have not resulted in improvements in the rural economy envisaged at their outset, not least because of failure to define development objectives and, in particular, development


objectives that are feasible under existing and predicted socio-economic conditions (Jordan, 1986).

Unfortunately in the past little attempt has been made to undertake economic analyses at the onset of control programmes against which economic impact could be assessed. In order to produce useful results, economic analyses must be used to estimate the costs and benefits of an existing or proposed investment in disease control (James, 1997). In the context of tsetse and trypanosomosis control, social and economic analyses to examine the resource linkages within farming systems, the relationships between trypanosomosis and livestock production, crop production, resource allocations and issues such as gender, poverty and population fluxes are needed. However, where economic analyses have been made as for example in Nigeria, tsetse eradication was shown to be highly profitable at both the local and national level (Putt et al., 1980) because of nearby people and their livestock who could take advantage of the opportunities presented by the removal of tsetse flies. However, the Nigerian situation is almost unique because the country's large, rapidly expanding human population created a demand for land in both the arable and livestock sectors. Elsewhere in Africa, human population densities are lower and the pressure on land is less, and hence exploitation of areas cleared of tsetse will be slower and less complete. However in many regions the population is expanding rapidly and this will lead to situations comparable to those in Nigeria in the foreseeable future (Jordan, 1986).

3.2. Integrated disease management

Trypanosomosis is only one of the many problems which threaten the survival and productivity of domestic livestock in Sub-Saharan Africa. Tick-borne diseases, helminthosis and viral diseases all cause major losses. Under-nutrition is equally threatening and the adverse effects of disease and under-nutrition are frequently com- pounded. There is therefore a need to assess the relative risks posed by these threats and develop cohesive and relevant strategies to minimise the risks involved.

Prior to the initiation of control schemes it is important to determine the level of impact of trypanosomosis on livestock survival and production. This judgement will depend on a variety of data, including mortality and morbidity rates, herd structure and reproductive performance and the presence and density of tsetse flies in the area. Diagnostic methods to determine the incidence and prevalence of trypanosomosis continue to lack adequate sensitivity and a combination of methods including fresh blood smears, buffy coat and haemotocrit examination, and stained thin and thick blood films are required. Serodiagnostic methods, for example ELISA, have some theoretical advantages over parasitological diagnosis, such as increased sensitivity, objectivity of testing and automation of data processing, but for various reasons none has yet seen widespread application.

Over many centuries nomadic pastoralists have developed integrated management strategies for minimising disease risk and maximising feed supply to their animals. Unfortunately, damp fertile areas which provide the best grazing are also the areas where the threats from tsetse flies, ticks and helminths are the greatest. Management strategies generally involve restricting grazing in these areas until late in the dry season


when the disease risk is lowest and the nutritional demands greatest. Such integrated management schemes are used by traditional cattle herders such as the Maasai and Fulani people, but may be put at risk by changes in land tenure patterns which may force them to abandon traditional nomadic life styles for a more settled existence.

In settled farming communities with mixed crop/livestock systems opportunities for avoiding tsetse infested areas are less and control schemes have to be implemented. At one extreme, zero grazing may be practised e.g. at the Kenyan coast by smallholder dairy farmers, and this reduces the risks from tsetse, ticks and helminths. However in most smallholder schemes grazing takes place and other prophylactic measures are required.

Programmes of integrated disease control may utilise techniques which control several vectors e.g. both tsetse and ticks, or several diseases e.g. the use of trypanocidal drugs which are also babesicidal. Synthetic pyrethroids can be used for the integrated control of ticks and tsetse flies. One such programme at a village in southwest Burkina Faso has been reported by Bauer et al. (1992b). The programme began with the block treatment of 2000 cattle with diminazene aceturate (7 mg kg-1 b.w.) followed by the application of flumethrin pour-on (1 mg active ingredient kg -~ b.w.) at monthly intervals. These resulted in a rapid decrease in the incidence of trypanosomosis to below 5% after 3 months and the average tick infestation was 3-10 times lower than a control site in spite of the repeated use of another acaricide at that site. In addition to tsetse flies and ticks other haematophagous insects such as tabanids, stomoxyine and nuisance flies were also affected by flumethrin. Reductions in their numbers can provide additional productivity benefits to cattle owners. Such types of integrated control have clear attractions both in disease control and economic returns.

Although trypanosomosis remains the most widespread threat to livestock in Sub- Saharan Africa there has been a tendency to focus resources on the control of this single disease at the expense of a broader integrated approach.

There is a need for more research into the impact of trypanosomosis relative to other constraints on livestock survival and productivity and evaluation of control possibilities at the local level in order that more effective integrated management practices can be developed.

3.3. Integration of tsetse and trypanosomosis control methods

In the past there has been heavy reliance by African countries on single control techniques and little attempt at integration of different methods. However experience from other disease control situations suggests that a combination of different methods may yield far greater benefits than a single method alone.

In pastoralist communities a combination of grazing practices (referred to earlier) with perhaps a single injection of a chemoprophylactic drug at the time of maximum tsetse challenge has been usual over many decades (Roderick, 1995). However new technologies especially in vector control are providing new and exciting possibilities for improved control by integrating various control measures. These include the integration of various methods of vector control and the integration of vector and parasite control strategies.

130 P.H. Holmes/Veterinary' Parasitology 71 (1997) 121-135

3.3.1. Integration of different methods of vector control In the past the use of different methods of tsetse control has generally been on a

sequential basis, e.g. in Burkina Faso and Zanzibar using insecticide impregnated screens or traps to significantly reduce tsetse fly numbers followed by the release of sterile males to bring about final elimination. (e.g. Cuisance et al., 1984). However in the accepted understanding of integrated pest management (IPM) the insect pest should be attacked simultaneously with a variety of interventions and this approach has rarely been applied to tsetse flies. It is therefore of interest that recently there have been limited attempts in Southern Africa to integrate stationary targets with insecticidal treatment of cattle.

The advantages of combining different vector control techniques certainly merits further study and evaluation.

3.3.2. Integration of drugs and tsetse control Chemoprophylactic drugs are most effective in areas with low-to-medium tsetse

challenge. When challenge reaches high levels the duration of prophylaxis is usually diminished (Whiteside, 1962). The reasons for this have remained uncertain but it is likely that in situations of high tsetse challenge the probability of an animal being infected with trypanosomes with innate or acquired drug resistance is enhanced and this will be manifest as a reduction in the duration of prophylaxis.

Moreover, there is recent evidence that once cattle become infected with drug-resistant trypanosomes, trypanocidal drug levels in the blood diminish at an accelerated rate and further reduce the protection provided by chemoprophylactic drugs (Eisler et al., 1994; Murilla, 1996).

As referred to earlier, at the Mkwaja Ranch in Tanzania under a good management system, a high level of production was maintained over a 27 year period using chemoprophylaxis and chemotherapy in an area where cattle would otherwise have died of trypanosomosis (Trail et al., i 985). The level of productivity achieved by a herd of about 12 000 Grade Boran cattle was about 80% of the level of the best Boran herds kept in a tsetse-free area of Kenya. However in areas of Mkwaja where an integrated trypanosomosis control approach was practised by the addition of bush clearing, spraying and tsetse trapping, levels of productivity were even better and equalled the average of that on Kenyan ranches (Trail et al., 1985).

In the late 1980s it became apparent at Mkwaja that the frequency and level of isometamidium treatment had to be increased in herds reliant on chemoprophylaxis alone. At this point dipping cattle in deltamethrin was started and this resulted in a rapid reduction in the tsetse population, reduced use of trypanocidal drugs and a marked improvement in herd health and productivity (Fox et al., 1993).

In situations of high tsetse challenge the reduced protection provided by trypanocidal drugs is likely to be due to the emergence of drug-resistant strains of trypanosomes. However this is rarely confirmed. One exception is the detailed study by scientists from the International Livestock Research Institute (ILRI) in the Ghibe Valley of Southwest Ethiopia. In a longitudinal study the epidemiology of bovine trypanosomosis was investigated between 1986 and 1990. Animals found to be parasitaemic and with a PCV less than 26% were treated with diminazene aceturate at a dose of 3.5 mg kg-~ body


weight. The majority of infections were associated with Trypanosoma congolense. The mean percentage of animals detected parasitaemic 1 month after treatment was 27%. A model was applied which allowed the monthly incidence of new infections to be distinguished from recurrent infections. The model showed that the monthly incidence of new infections increased significantly from 11% in 1986 to 24% in 1989 following a concomitant increase in the tsetse challenge. However it was suspected that the rise in prevalence rate was not only due to the high tsetse challenge but also drug-resistant strains of T. congolense (Rowlands et al., 1993). Ten isolates of T. congolense collected at random were all shown to be resistant to the recommended doses of diminazene, isometamidium and homidium (Codjia et al., 1993).

With such a high incidence of drug resistance, a higher trypanosome prevalence might have been expected in village cattle. Thus, whilst treatment was not eliminating infections, it may have helped to limit the trypanosome growth and allowed the cattle to maintain reasonable levels of health and productivity. This was confirmed by statistical analysis of the productivity data (Mulatu et al., 1993). Although there were statistically significant effects of trypanosomosis on productivity the effects were generally small or transient. The most significant effect of trypanosomosis appeared to be on calf and foetal mortality, particularly during periods of very high tsetse challenge, or increased trypanosomosis risk brought about by other stress-related factors.

Economic analysis showed that cattle production in the Ghibe Valley could generate attractive returns for herd owners despite the high level of trypanosomosis risk and the prevalence of drug-resistant trypanosomes. Sensitivity analyses showed that most herd owners would continue to obtain good returns on their investments even if they paid higher prices for trypanocidal drugs and the full costs of veterinary services (Itty et al., 1995).

Because of the high incidence of drug resistance and the detrimental effects of trypanosomosis on young stock at Ghibe, a tsetse control programme was initiated in 1990 using odour-baited deltamethrin-impregnated targets placed across the entire valley at an average density of 4 km- 2. Diminazene treatment continued on an individual basis as previously. As a result of the tsetse control measures the relative density of the main vector, Glossina pallidipes, fell from a mean of 1.9 flies per trap per day to 0.09 flies per trap per day and the apparent prevalence of T. congolense infections in cattle fell from approximately 30% to a mean of 5% (Leak et al., 1996). Moreover, and of particular interest, the prevalence of diminazene-resistant infections appeared to decrease by approximately 75% in the first 12 months following initiation of the tsetse-control programme (Peregrine et al., 1994) and clearly demonstrated the benefits of integrated control.

Unfortunately the theft of a large number of targets in 1991 spoiled the major reductions in tsetse density and trypanosome prevalence which had been achieved. Instead of targets a pour-on insecticide programme using cypermethrin was initiated and for 2 years (1991-1992) was freely provided. In late 1992 a charge of approximately US$1 was levied to cover the costs of purchasing and administering the treatments. Nevertheless farmers appreciated the benefits of the pour-on and continued to be willing to pay for monthly applications (Swallow et al., 1995). The perceived advantages included less trypanosomosis, fewer problems with ticks, the animals grazed well and


quietly, cows were quieter when milking, there were fewer problems with ox peckers bothering the animals and the animals' wounds healed faster.

By 1993 there had been a decline of 93% in the apparent density of G. pallidipes and 83% of G. morsitans submorsitans. The numbers of Stomoxys spp. and Tabanidae were also significantly reduced (Leak et al., 1995).

3.3.3. Integration of trypanotolerance with drugs In West Africa especially, trypanotolerant breeds of cattle can thrive in tsetse-ende-

mic areas in which less tolerant breeds such as Zebu succumb to trypanosomosis. However it has been shown that trypanotolerant cattle are best suited to situations with low to medium challenge. In areas of high challenge the detrimental effects of trypanosomosis often become apparent and the use of trypanocidal drugs may be required e.g. in Mali (Diall et al., 1992) and Gabon (Trail et al., 1993). It is likely that trypanocidal drugs are commonly used throughout West Africa in trypanotolerant breeds to protect valuable animals such as work oxen although their use is rarely documented. Further studies to evaluate the use of trypanocidal drugs in trypanotolerant breeds are required.

3.3.4. Integration of trypanotolerance and tsetse control There are few reports of the integration of trypanotolerant cattle with tsetse control

although the recently developed bait technologies offer new forms of integrated control. One study in the Gambia using a deltamethrin application on N'dama cattle is currently being undertaken and the initial results are encouraging. The combined benefits of tsetse and tick control with reductions in the populations of biting and nuisance flies may prove to be attractive to livestock owners, especially if the number of applications of insecticide each year is small.

3.3.5. Integrated control of human and animal trypanosomosis There is now considerable evidence that cattle can act as a reservoir of one of the

parasites that causes human trypanosomosis, T. brucei rhodesiense. A recent study by Angus (1996) in Western Kenya investigated the epidemiology of T. brucei spp infections in cattle and the potential for controlling both the reservoir of human trypanosomosis and pathogenic infections with T. congolense and T. vivax by the use of the chemoprophylactic drug, isometamidium. In the study area tsetse control by impregnated traps had been implemented in the early 1990s and achieved an apparent reduction of the tsetse fly population of over 99% yet the prevalence of T. brucei spp infections remained high (up to 26%) in cattle as did infections with T. vivax and T. congolense. However following block treatment with isometamidium, existing infections were eliminated and 94% protection was provided for at least 3 months. A significant increase in the mean PCV and liveweight gain of the cattle was observed during the period of prophylaxis (Angus et al., 1995). This integrated approach to the control of both the reservoir of human trypanosomosis and animal trypanosomosis by chemoprophylaxis clearly may have future applications in endemic areas.

3.3.6. The future Integrated approaches to the control of tsetse and trypanosomosis have many

attractions and are expected to receive greater attention in the future. They are

P.H. Holmes//Veterinary Parasitology 71 (1997) 121-135 133

particularly appropriate when effective suppression rather than eradication is the desired objective. However a more detailed evaluation of the relationship between tsetse population densities and the occurrence of disease is required. It is also necessary to determine the type and degree of intervention required to maintain acceptable levels of disease suppression.

Across Africa there is growing interest in transferring tsetse control services and veterinary services to the private sector in order to improve their sustainability. Veterinary privatisation schemes are now underway in several countries and frequently have significant donor support. Although agreed as a policy there are considerable difficulties in their implementation and it is too early to know how successful these measures will be. There is also an ongoing debate as to which duties should be retained by the government e.g. the monitoring/supervision of private sector activities, control of notifiable diseases, quarantine requirements etc. (Putt et al., 1993). It is expected that in addition to private and state services a third sector will emerge consisting of organisations which are able to provide services for the common benefit of their members (Holden et al., 1996).

Privatisation of tsetse control and veterinary services can be expected to have a significant effect on the implementation of integrated control programmes against trypanosomosis in the future.

The challenge for all those concerned with tsetse and trypanosomosis control in Africa is to develop methods which are sustainable, appropriate, cost-effective and integrated with rural development. These can only be achieved through farmer motivation and education, improved delivery of tsetse control and veterinary services, commer- cial opportunities and cost recovery schemes, whilst at the same time encouraging the pharmaceutical industry and the scientific community to search for new drugs and an effective vaccine against this most devastating of diseases.

Acknowledgements

The author gratefully acknowledges the contribution to this review by his colleagues through many valuable discussions on the control of trypanosomosis. The work of the author and his group described in this review was supported by the British Overseas Development Administration and EU DGXII Science, Research and Development.

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New approaches to the integrated control of trypanosomosis