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.     

The effect of trypanosomosis on pregnancy in trypanotolerant Orma Boran cattle

A study was undertaken to investigate the influence of trypanosomosis on the outcome of pregnancy in trypanotolerant Orma Boran (Bos indicus) exposed to natural tsetse challenge in an area of Kenya infested predominantly with Glossina pallidipes. Of 73 pregnant Orma heifers, 58 (79.5%) produced live calves at term, 13 (17.8%) aborted and 2 (2.7%) died of trypanosomosis. Of the 71 surviving animals, 22 (31%) were infected with Trypanosoma vivax , 21 (29.6%) T. congolense, and 26 (36.6%) had mixed infections with T. vivax and T. congolense. These results suggest that in areas of high trypanosomosis risk reproductive function is affected even in trypanotolerant cattle, and that both T. vivax and T. congolense can be responsible for the abortions observed in the field. It is suggested that maintenance of pregnancy in the face of trypanosome challenge was dependent on individual variation among the Orma cattle, but as challenge increased beyond the limits of effectiveness of trypanotolerance, disruption of pregnancy occurred.     

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.     

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.     

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.     

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.     

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.     

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.     

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.     

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.     

Use of deltamethrin 'pour-on' insecticide for the control of cattle trypanosomosis in the presence of high tsetse invasion

A deltamethrin 'pour-on' insecticide was applied monthly to over 2000 cattle exposed to a high challenge of drug-resistant trypanosomes and high tsetse re-invasion pressure in the Ghibe valley, south-west Ethiopia. Blood samples were taken monthly from an average of 760 cattle for determination of PCV and presence of trypanosomes. The area of the valley is approximately 350 km2 and the cattle grazed in roughly four locations covering about a quarter to half of the area. Two years before the trial commenced, Glossina morsitans submorsitans Newstead (Diptera: Glossinidae) began to invade the valley. Despite the use of the pour-on the mean apparent density of G. m. submorsitans continued to rise, and, during the 4 years of tsetse control, was more than three-fold higher than that recorded during the previous 18 months. Over the same period there was little change in the apparent density of Glossina pallidipes Austen (Diptera: Glossinidae). By contrast, the mean monthly prevalence of trypanosome infections in cattle over 36 months of age decreased from 38.3 to 29.0%, the incidence of new infections decreased from 26.6 to 16.0% (a reduction of 40%), and packed cell volume in cattle increased from 21.7 to 24.1%. Evidence of a change in apparent parasite transmission rate was demonstrated by regression of infection incidence in cattle on the logarithm of apparent density of G. m. submorsitans. Before the trial started the regression coefficient was 45.8 +/- 6.3 and this reduced to 9.2 +/- 2.5% incidence per log(e) (flies/trap/day) during the period of tsetse control. It was concluded that this indicated reductions in tsetse numbers in the immediate vicinities of cattle in a way that was not reflected in overall tsetse catches. Nevertheless, the comparatively high levels of trypanosome prevalence that persisted in the cattle demonstrates that, where invasion prevalence is high, treatment of small pockets of cattle will not eradicate tsetse. To achieve more significant reduction in trypanosome prevalence in cattle, integrated methods of control utilizing target barriers in the major routes of invasion will be needed.     

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.     

The effects of host physiology on the attraction of tsetse (Diptera: Glossinidae) and Stomoxys (Diptera: Muscidae) to cattle

In Zimbabwe, studies were made of the numbers of tsetse (Glossina spp.) and stable flies (Stomoxys spp.) attracted to cattle of different nutritional status, age and sex. Host odours were analysed to determine the physiological basis of these differences and improved methods are described for measuring rates of production of kairomones. Seasonal fluctuations in host weight, related to changes in pasture quality, had no significant effect on attraction of tsetse or Stomoxys. However, both attraction to different individuals and carbon dioxide production by these individuals were strongly correlated with weight, suggesting a possible link. Attraction to the odour from different types of cattle decreased in the order ox>cow>heifer>calf, and oxen were twice as attractive as calves of less than 12 months old. Lactation did not alter the relative attractiveness of cows. Calves less than six months old produced lower levels of carbon dioxide, acetone, octenol and phenols than oxen, but for older calves and cows, levels of production of known kairomones and repellents were similar to those of an ox. Carbon dioxide produced by cattle varied according to time of day and the animal's weight; cattle weighing 500 kg produced carbon dioxide at a mean rate of 2.0 l min(-1) in the morning and 2.8 l min(-1) in the afternoon compared to respective rates of 1.1 and 1.9 l min(-1) for cattle weighing 250 kg. Artificially adjusting the doses of carbon dioxide produced by individual cattle to make them equivalent did not remove significant differences in attractiveness for tsetse but did for Stomoxys. Increasing the dose of carbon dioxide from 1 to 4 l min(-1) in a synthetic blend of identified kairomones simulating those produced by a single ox, increased attractiveness to tsetse but not to the level of an ox. The results suggest that the main sources of differences in the attractiveness of individual cattle are likely to be variation in the production of carbon dioxide and, for tsetse, other unidentified kairomone(s). The biological and practical implications of these findings are discussed.     

Glossina fusca group tsetse as vectors of cattle trypanosomiasis in Gabon and Zaire

1. The significance of Glossina fusca group tsetse flies as vectors of cattle trypanosomiasis was examined using biconical traps to survey tsetse populations at one site in Gabon and two sites in Zaire. 2. Mean trypanosome infection rates in G.tabaniformis Westwood over the study period ranged from a minimum of 8.9% at one site to a maximum of 17.7% at another. The mean infection rate in G.nashi Potts was 6.0%. 3. Up to 49% of bloodmeals of G.tabaniformis were from cattle. Trypanosome prevalence in cattle where G.tabaniformis appeared to be the main vector was 9.5% and 5.4% at the Mushie and OGAPROV ranches, respectively. 4. A highly significant positive correlation was found between tsetse challenge and trypanosome prevalence in N'Dama cattle across sites. Tsetse challenge was defined as the product of tsetse relative densities, trypanosome infection rates in the flies and the proportion of feeds taken by them from cattle. Thus, G.tabaniformis can be an important vector of pathogenic Trypanosoma species in cattle.     

Prospects for control of African trypanosomiasis by tsetse vector manipulation

The extensive antigenic variation phenomena African trypanosomes display in their mammalian host have hampered efforts to develop effective vaccines against trypanosomiasis. Human disease management aims largely to treat infected hosts by chemotherapy, whereas control of animal diseases relies on reducing tsetse populations as well as on drug therapy. The control strategies for animal diseases are carried out and financed by livestock owners, who have an obvious economic incentive. Sustaining largely insecticide-based control at a local level and relying on drugs for treatment of infected hosts for a disease for which there is no evidence of acquired immunity could prove extremely costly in the long run. It is more likely that a combination of several methods in an integrated, phased and area-wide approach would be more effective in controlling these diseases and subsequently improving agricultural output. New approaches that are environmentally acceptable, efficacious and affordable are clearly desirable for control of various medically and agriculturally important insects including tsetse. Here, Serap Aksoy and colleagues discuss molecular genetic approaches to modulate tsetse vector competence.     

Control of tsetse and trypanosomiasis transmission in Uganda by applications of lambda-cyhalothrin

The pyrethroid insecticide lambda-cyhalothrin was evaluated in field trials against Glossina f.fuscipes and sleeping sickness transmission in Iyolwa sub-county, Tororo District, Uganda. The insecticide was applied selectively to the resting-sites of tsetse, by bush-spraying, using 10% wettable powder (10WP) formulation at an application rate of 11.6 g a.i./ha over an area of 28 km2, or by a 2% Electrodyn formulation (2ED) applied at 0.9 g a.i./ha over 30 km2. In a third trial area of 32 km2, 215 pyramidal traps treated with lambda-cyhalothrin 100 mg/m2 were set. The best impact was obtained with 10WP lambda-cyhalothrin which eliminated tsetse within 1-2 months, whereas G.f.fuscipes persisted at very low density in part of the area treated with 2ED lambda-cyhalothrin. In both treated areas the numbers of human sleeping sickness cases fell to no more than one per month, compared with four to twelve per month previously. The overall rate of cattle trypanosomiasis (T.brucei and T.vivax) was also reduced slightly. Insecticide-treated traps remained fully effective for at least 6 months under field conditions and catches were reduced 20-90-fold. These results in the control of tsetse and trypanosomiasis transmission lead us to recommend lambda-cyhalothrin for tsetse control operations.     

Factors associated with acquisition of human infective and animal infective trypanosome infections in domestic livestock in Western Kenya

Background

Trypanosomiasis is regarded as a constraint on livestock production in Western Kenya where the responsibility for tsetse and trypanosomiasis control has increasingly shifted from the state to the individual livestock owner. To assess the sustainability of these localised control efforts, this study investigates biological and management risk factors associated with trypanosome infections detected by polymerase chain reaction (PCR), in a range of domestic livestock at the local scale in Busia, Kenya. Busia District also remains endemic for human sleeping sickness with sporadic cases of sleeping sickness reported.

Results

In total, trypanosome infections were detected in 11.9% (329) out of the 2773 livestock sampled in Busia District. Multivariable logistic regression revealed that host species and cattle age affected overall trypanosome infection, with significantly increased odds of infection for cattle older than 18 months, and significantly lower odds of infection in pigs and small ruminants. Different grazing and watering management practices did not affect the odds of trypanosome infection, adjusted by host species. Neither anaemia nor condition score significantly affected the odds of trypanosome infection in cattle. Human infective Trypanosoma brucei rhodesiense were detected in 21.5% of animals infected with T. brucei s.l. (29/135) amounting to 1% (29/2773) of all sampled livestock, with significantly higher odds of T. brucei rhodesiense infections in T. brucei s.l. infected pigs (OR = 4.3, 95%CI 1.5-12.0) than in T. brucei s.l. infected cattle or small ruminants.

Conclusions

Although cattle are the dominant reservoir of trypanosome infection it is unlikely that targeted treatment of only visibly diseased cattle will achieve sustainable interruption of transmission for either animal infective or zoonotic human infective trypanosomiasis, since most infections were detected in cattle that did not exhibit classical clinical signs of trypanosomiasis. Pigs were also found to be reservoirs of infection for T. b. rhodesiense and present a risk to local communities.     

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.