Tsetse Control and Gambian Sleeping Sickness; Implications for Control Strategy.

BACKGROUND: Gambian sleeping sickness (human African trypanosomiasis, HAT) outbreaks are brought under control by case detection and treatment although it is recognised that this typically only reaches about 75% of the population. Vector control is capable of completely interrupting HAT transmission but is not used because it is considered too expensive and difficult to organise in resource-poor settings. We conducted a full scale field trial of a refined vector control technology to determine its utility in control of Gambian HAT. METHODS AND FINDINGS: The major vector of Gambian HAT is the tsetse fly Glossina fuscipes which lives in the humid zone immediately adjacent to water bodies. From a series of preliminary trials we determined the number of tiny targets required to reduce G. fuscipes populations by more than 90%. Using these data for model calibration we predicted we needed a target density of 20 per linear km of river in riverine savannah to achieve >90% tsetse control. We then carried out a full scale, 500 km2 field trial covering two HAT foci in Northern Uganda to determine the efficacy of tiny targets (overall target density 5.7/km2). In 12 months, tsetse populations declined by more than 90%. As a guide we used a published HAT transmission model and calculated that a 72% reduction in tsetse population is required to stop transmission in those settings. INTERPRETATION: The Ugandan census suggests population density in the HAT foci is approximately 500 per km2. The estimated cost for a single round of active case detection (excluding treatment), covering 80% of the population, is US$433,333 (WHO figures). One year of vector control organised within the country, which can completely stop HAT transmission, would cost US$42,700. The case for adding this method of vector control to case detection and treatment is strong. We outline how such a component could be organised.

Where, when and why do tsetse contact humans? Answers from studies in a national park of Zimbabwe.

BACKGROUND: Sleeping sickness, also called human African trypanosomiasis, is transmitted by the tsetse, a blood-sucking fly confined to sub-Saharan Africa. The form of the disease in West and Central Africa is carried mainly by species of tsetse that inhabit riverine woodland and feed avidly on humans. In contrast, the vectors for the East and Southern African form of the disease are usually savannah species that feed mostly on wild and domestic animals and bite humans infrequently, mainly because the odours produced by humans can be repellent. Hence, it takes a long time to catch many savannah tsetse from people, which in turn means that studies of the nature of contact between savannah tsetse and humans, and the ways of minimizing it, have been largely neglected. METHODOLOGY/PRINCIPAL FINDINGS: The savannah tsetse, Glossina morsitans morsitans and G. pallidipes, were caught from men in the Mana Pools National park of Zimbabwe. Mostly the catch consisted of young G. m. morsitans, with little food reserve. Catches were increased by 4-8 times if the men were walking, not stationary, and increased about ten times more if they rode on a truck at 10 km/h. Catches were unaffected if the men used deodorant or were baited with artificial ox odour, but declined by about 95% if the men were with an ox. Surprisingly, men pursuing their normal daily activities were bitten about as much when in or near buildings as when in woodland. Catches from oxen and a standard ox-like trap were poor indices of the number and physiological state of tsetse attacking men. CONCLUSION/SIGNIFICANCE: The search for new strategies to minimize the contact between humans and savannah tsetse should focus on that occurring in buildings and vehicles. There is a need to design a man-like trap to help to provide an index of sleeping sickness risk.

Shoo fly, don't bother me! Efficacy of traditional methods of protecting cattle from tsetse.

Studies were made of the efficacy of using smoke and housing to protect cattle from tsetse (Diptera: Glossinidae) in Zimbabwe. The efficacy of smoke was assessed by its effect on catches in Epsilon traps baited with a blend of acetone, 1-octen-3-ol, 4-methylphenol and 3-n-propylphenol. The efficacies of different types of kraal (enclosure) were gauged according to the catches of electrocuting targets (E-targets), baited with natural ox odour, placed within various designs of kraal. Smoke from burning wood (Colophospermum mopane) or dried cow dung reduced the catch of traps by approximately 50-90%. Kraals with a continuous wooden or netting wall, 1.5 m high, reduced catches of E-targets by approximately 75%. Arrangements of electric nets were used to assess the numbers of tsetse attacking live cattle within kraals and/or near sources of smoke. The results confirmed findings with traps and E-targets: kraals reduced the numbers of tsetse that fed by approximately 80% and smoke reduced the numbers attracted by approximately 70%; the use of both reduced overall attack rates by approximately 90%. The inclusion of 4-methylguaiacol, a known repellent for tsetse and a natural component of wood smoke, halved the catches of traps and E-targets and the numbers of tsetse attacking cattle. The practical benefits and difficulties of using repellents and/or housing to manage trypanosomiases are discussed.

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.

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

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

Interactions between cattle and biting flies: effects on the feeding rate of tsetse.

In Zimbabwe, studies were made of the effect of host behaviour on the feeding success of Glossina pallidipes Austen and G. morsitans morsitans Westwood (Diptera: Glossinidae) attracted to cattle of different age and sex. The mean feeding rates for male and female G. pallidipes attracted to oxen were 60% and 58%, respectively, compared to 33% and 53% for male and female G. m. morsitans. The feeding rate of G. pallidipes varied between oxen and was inversely correlated with a host's rate of defensive leg movements, which, in turn, was positively correlated with the density of Stomoxys spp. (Diptera: Muscidae) caught in the vicinity of the host. Tsetse were significantly less successful in feeding from young cattle. For G. pallidipes, the feeding rate on calves (<6 months) was 11%, whereas for male and female G. m. morsitans the rates were 12% and 20%, respectively. Significantly lower feeding rates were apparent for cattle aged up to 2 years, when the feeding rate for G. pallidipes (31%) was still significantly less than that on mature oxen (68%). Feeding rates for G. pallidipes on adult female cattle were lower than those on oxen (45% vs. 61%). The lower feeding rates in young animals were attributed to higher rates of defensive movements. The results suggest that higher rates of defensive activities by young cattle reduce the risk of them contracting trypanosomiasis.

The efficacy of various pyrethroid insecticides for use on odour-baited targets to control tsetse.

The efficacy of various pyrethroid insecticides for use on odour-baited targets to control tsetse was compared in Zimbabwe. Formulations were applied to cotton cloth and polyester net and, at various intervals, the materials were bioassayed by exposing fed female Glossina pallidipes (Austen) (Diptera: Glossinidae) to cloth for 45 s or by inducing them to collide briefly with net. Trial formulations were compared with deltamethrin suspension concentrate (s.c.), the insecticide currently used in tsetse control operations in Zimbabwe. Applying 0.8% suspension of alphacypermethrin to cloth or net produced high mortalities for 9 months which was similar in performance to 0.4% suspension of deltamethrin s.c. Deltamethrin s.c. and beta-cyfluthrin s.c. applied to cloth as 0.1% suspensions were equally effective, producing high mortalities for 2 months during the wet season, and 0.8% suspension of beta-cyfluthrin was effective for 12 months. Suspensions of 0.1% lambdacyhalothrin capsule suspension or 0.1% lambdacyhalothrin wettable powder were significantly less effective than 0.1% deltamethrin s.c. Chemical analyses showed that increasing the concentration of insecticide applied to material increased the initial amount of insecticide on the material and decreased the subsequent rate of loss; 0.1% suspension of beta-cyfluthrin s.c. applied to cloth produced an initial concentration of approximately 280 mg/m2 which declined by 94% in 12 months whereas 0.8% suspension showed no significant decrease in concentration (mean= 1304 mg/m2) over the same period. For controlling tsetse by means of pyrethroid-treated targets, it is suggested that beta-cyfluthrin s.c. is as effective as deltamethrin s.c. but that alphacypermethrin s.c. should be used at twice the concentration of deltamethrin s.c. to obtain the same performance.