Trypanosomiasis epidemiologyM. CLAIR
Introduction
The parasite - The trypanosome
The vector - The tsetse fly
The host - The animal
The human factor
General points
Conclusion
References
Three elements influence the epizootiology of African animal trypanosomiasis, namely: the trypanosome, the tsetse fly and the animal itself. Many studies have been done and are presently underway on each of these elements. Any discovery, even if it is only partial, leads not only to a better understanding of this complex group (parasite-vector-host and their multiple interactions) but also to a better control of the disease.
This paper will concentrate on the trypanosomes which are cyclically transmitted by tsetse. Apart from the tsetse, which is the main vector of trypanosomiasis, other biting insects can transmit the disease (Tabanidae, Muscidae, Hippoboscidae) through interrupted blood meals. This "mechanical transmission" is difficult to study and there is still little information on it. It concerns primarily T. vivax which is also transmitted cyclically. This phenomenon undoubtedly plays a role in the dispersion and growth of the disease. However in the absence or disappearance of tsetse it becomes less serious. This has been evident in the Sideradougou area (Centre de Recherches sur les Trypanosomes Animales [CRTA], Burkina Faso) where only T. vivax is still found, although at a very low density (Bauer et al., in press).
T. evansi is found in abundance in much drier zones and is transmitted only by other biting flies. It causes surra which leads to high mortality in camels in North Africa and in Eastern Africa (Sudan, Ethiopia). The study of this trypanosome, which had been neglected for a long time, has regained interest in recent years. The International Working Group on T. evansi infections which meets once or twice a year is a good example, especially at the annual meeting of the Office International des Epizooties (OIE) in Paris (OIE, 1987).
Finally, let us mention T. theileri which is found worldwide in cattle. It is non-pathogenic and is transmitted by tabanids. T. equiperdum causes dourine and is transmitted through copulation.
The studies cited here mainly concern the two principal cyclically transmitted trypanosomes in cattle, Trypanosoma congolense and Trypanosoma vivax and to a lesser degree Trypanosoma brucei. Although T. brucei brucei only has secondary effects in cattle, T. brucei gambiense is of considerable importance to humans as it causes sleeping sickness in West and Central Africa. Finally, let us mention T. simiae which is rare but very pathogenic to pigs and T. suis which is found only in domestic and wild suids.
ILCA/ILRAD's ATLN is engaged in numerous epidemiological studies and some results have already been obtained: trypanosome prevalence is higher (sometimes twice as high) in N'Dama cattle than in Djallonke sheep (Togo and Cote d'Ivoire) (Defly et al., in press; Schuetterle et al., in press). Percentage of T. vivax infections compared to T. congolense infections decreases with age in cattle (Mulungo et al., in press; Schuetterle et al., in press). T. vivax is significantly more frequent in sheep than in cattle (Schuetterle et al., in press). However many problems are still more or less unsolved including the estimation of infection rate in herds, a very important factor. Methods of trypanosome detection by examination of thick and thin blood smears and micro-centrifugation are inadequate. A rapid, reliable and cheap field test needs to be devised. Problem areas include multiple T. vivax and T. congolense infections in cattle and T. congolense and T. brucei infections in pigs; for example, how do they interact? Similarly, how can T. simiae and T. congolense be differentiated in pigs and T. brucei brucei and T. brucei gambiense in cattle?
Trypanosome strains must therefore be characterised and many techniques have been used to do this, including iso-enzymes as genetic markers, the direct analysis of DNA of the nucleus and of the kinetoplast and the production of highly specific monoclonal antibodies (Gibson et al., 1985). These methods and serological tests (ELISA, B.I.I.T.) have shown the existence of an animal reservoir for T. brucei gambiense and a new classification has been proposed (Gibson et al., 1985; Mehlitz, 1986; Vickerman, 1985).
All the stages of the parasites have not been cultivated and a technique to produce a large number of metacyclical forms (Brun and Jenni, 1985) is still to be developed. Much research has been done on the biochemical peculiarities of trypanosomes (Opperdoes, 1985) and on the biochemistry of surface antigens (IEMVT, 1985; Turner, 1985).
It is evident that disease risk depends primarily on the density of the vector. All factors influencing tsetse populations, disease risk and consequently the evolution of the disease should be considered i.e., climatic and ecological factors, presence of trypanosomes, food sources (hosts), etc.
Disease Risk
The study of trypanosomiasis risk is recent and ILCA/ILRAD's ATLN is presently trying to evaluate this risk using three components: tsetse relative density, trypanosome infection rate and proportion of blood meals taken from livestock in the study. The index obtained from these three traits is compared with trypanosome prevalence in cattle (Leak et al., in press). More information is being collected to improve the correlation.
There is little accurate information on the rate of infection in flies (analyzed by dissecting the flies), even though it is a very important factor for measuring risk. When DNA probes for identification of trypanosome species are brought to perfection our knowledge should improve greatly (Gibson, in press).
Environmental factors
Climatic variations have a direct impact on tsetse distribution. The recent droughts in west Africa and the ensuing migration of people towards the south (resulting in the destruction of vegetation and fauna) have caused a regression in tsetse: G. tachinoides has now receded to the intermediate zone between the forest and the savanna in Cote d'Ivoire and G. morsitans submorsitans and G. tachinoides are very rare in the "W" park in Niger and Burkina Faso (Clair and Lamarque, 1984; Clair, 1986; Clair, 1987; Katondo, 1984).
Vector/parasite relationships
The occurrence of different strains within the same tsetse population (with regard to their power to transmit trypanosomes) has led to the study of the genetic and physiological explanations of receptivity to trypanosome infections in tsetse (Maudlin, 1985; Maudlin and Dukes, 1985).
This is a stable trait transmitted by the female but is not absolute; all receptive tsetse do not become infected. Other factors are involved, such as age of the tsetse, quality of blood absorbed (depending on whether it contains lipoproteins or serum) and presence of rickettsia-like organisms (RLOs). Sensitive strains have a lot of rickettsia localised in cells of the middle intestines near the mycetome and therefore play an important role in metabolism. Strains of tsetse without rickettsia are refractory to trypanosomes. Viral particles also seem to have an influence. Their presence seems to cause resistance to infection. The Bristol TRL has selected strains of G. p. palpalis and of G. m. morsitans which are receptive to infection and available to researchers. It is also known that the Salmon mutant of G.m. morsitans has a higher vectorial capacity than the wild species (Makumyaviri et al., 1984).
When little was known about reactions of tsetse to trypanosomes it seemed as though they were unaffected. This is not true and there are several facts which contradict this idea. Parasitaemic flies are more sensitive to insecticides (Colder and Miles, 1984; Nitcheman, 1985) than uninfected flies. Scientists are beginning to investigate the haemocoele of tsetse and its role with respect to external agents. A trypanosomal factor has been discovered in the haemolymph of several tsetse species (Croft et al., 1982). Humoral and cellular defence reactions of G.m. morsitans against bacteria and T. brucei brucei were studied. Haemocytes have a phagocytic action on foreign bodies and the level of certain proteins increases. A small quantity of injectable E. cold can be used as an effective vaccine. Parasite haemagglutines and agglutines which could be lectins have also been discovered in the haemolymph and the intestines of tsetse (Kaaya et al., 1986a,b) Therefore tsetse flies have effective defence mechanisms against external attacks and consequently against trypanosomes, which constitute a considerable percentage of tsetse infections.
Little is known about the trypanosomal cycle in flies, passage through the haemocoele, identification of cyclical forms (Vickerman, 1985) etc. The diagnosis could be improved by application of specific DNA probes (Gibson, in press; Gibson et al., 1985).
Ecological factors
During thorough epidemiological surveys on sleeping sickness in Cote d'Ivoire and the Congo, tsetse ecology was studied by Office de la Recherche Scientifique et Technique Outre-Mer (ORSTOM). Research (especially on physiology) which explains tsetse ecology is discussed here.
Tsetse do not have volatile pheromones with a long range effect as is the case for other insects (Lepidoptera...). However, all species seem to have cuticular hydrocarbons which act at close range and which cause males to copulate (Carlson and Langley, 1986; Messoussi and Jallon, 1987; Okoth and Phillips, in press). Attempts have been made to control tsetse flies by impregnating traps with this pheromone combined with a chemosterilant (Langley et al., 1982).
A certain number of substances were measured in tsetse, such as fats, in order to find out the hunger stage and the level of pteridine in the head in order to estimate the age of the fly.
Many studies focussed on establishing tsetse behaviour with regard to traps (visual, olfactory). Remarkable results were obtained. A large number of models of traps and screens were made (by Veterinary Services in Zimbabwe and by ORSTOM in West Africa). These devices were so efficient that they were used in large-scale tsetse control campaigns in Cote d'Ivoire (at Vavoua and in the livestock zone in the North, 1983), in Burkina Faso (Sideradougou zone, 1983) and in the Congo (at Niari, 1986).
The discovery of odour attractants (acetone, octenol, phenol, in particular) has greatly increased the efficiency of baits. The attractants, which were first used in Zimbabwe on savanna tsetse, were equally efficient for catching the morsitans species in West Africa (IEMVT, 1985). Very recently it was discovered that riverine flies (palpalis group) were also attracted by certain odours (Merot et al., 1986; Merot et al., 1987).
Movement capacity of G.p. gambiensis (22 km) and G. tachinoides (25 km) along gallery forests was measured in Burkina Faso (Cuisance et al., 1985).
Research is making progress in all fields but much is still to be discovered.
The epizootiology of animal trypanosomiasis is extremely complicated because the disease affects not only cattle, but also and even to a greater extent, wild animals which constitute omnipresent reservoirs of the disease.
It is therefore tempting to destroy wild animals in order to eliminate both the reservoir and the parasite. With the disappearance of flies, cattle could be introduced. This method, which was used in West and Central Africa in the early days, has many disadvantages and is no longer acceptable.
In areas where there are few wild animals, increased cattle populations increase tsetse density to such a degree that eventually livestock farmers have to move to healthier areas. This has happened several times in the Central African Republic and shows the importance of animal hosts.
Analysis of tsetse bloodmeals provides valuable information on sources of feeds; trophic preferences are therefore well known but can vary depending on the availability of animals. This is one of the factors utilized by the ATLN to determine livestock performance with regard to the disease.
Following are some of the results ATLN has obtained:
- two or more trypanosome infections reduce calving rate of N'Dama's by a third (Ordner et al., in press).- the effect of repeated infections seems to be cumulative and PCV which reveals anaemia could be a useful indicator of trypanosome infection.
- cows have more T. congolense than T. vivax infections but the reverse is true of calves. Infections do not decrease the weight of the cow at parturition but decrease the weight of the calf at birth (Mulungo et al., in press).
- the effect of trypanosome infections on PCV is not increased by blood parasites, but is increased by internal parasites (Coulibaly et al., in press). Concomitant Theileria spp. infections are independent. More information is needed to determine, more precisely, interactions with helminths and other protozoa.
All this information allows the comparison of productivity of taurine breeds and zebus and the testing of their performance in infested areas.
The mechanism, transmission and limitations of trypanotolerance are only mentioned here.
Another method of control is the treatment of infected animals or their protection by chemoprophylaxis. This is an easy solution but runs the risk of creating of chemoresistant strains.
There is one last important factor to be taken into consideration, i.e. the human factor, which interferes the most in this complex group. Tsetse control cannot succeed fully unless it is done by the livestock owners themselves. For example, uncontrolled movement of livestock from infested to uninfested areas has brought back flies in the Admaoua plateau in the Cameroon. Another example: when traps and screens are used in anti-tsetse campaigns, neighbouring populations must be warned so that they participate fully, otherwise thefts and destruction are frequent.
As we have seen, chemotherapy if not applied properly, can lead to chemoresistance of certain strains. Therefore man, during his attempts to eradicate trypanosomiasis, prevents the natural development of the disease.
Man has more and more information on modes of transmission of the parasite. He therefore has more ways of taking action on all fronts, i.e. destroy or reduce the vector, treat and protect livestock, use trypanotolerant breeds. But in practice, the control campaign is making no headway. Each technique has its disadvantages and the high cost involved often reduces the number and scale of operations. Widespread insecticide spraying pollutes the environment. Chemotherapy often leads to the creation of resistant trypanosome strains.
Further, despite immense progress, the exact epidemiology of animal trypanosomiasis is still poorly understood for several reasons. Clinical diagnosis is difficult as there may be no pathogenic signs. Detection of trypanosomes is the only proof of the disease and for this a minimal number of instruments are needed including a microscope. Often, however, these instruments are not available, or are incomplete, or don't work. The work is enormous and the means are not always adequate. Furthermore, the diagnosis of the disease often depends only on clinical signs, or claims by the owner of the infected animal. In practice, treatment as a precaution is preferable even without experimental diagnosis. This explains the great number of trypanocides used sometimes in zones which have relatively low tsetse challenge. As a result of these factors, statistics from several countries on the number of breeding habitats, infected animals and deaths are unreliable.
It is therefore necessary to continue research and ensure that information on trypanosomiasis is gathered over a wide area and is as accurate as possible.
Although research has made much progress much more information is needed on interactions between trypanosomes and tsetse (immune system), between trypanosomes and the host (trypanotolerance) and between the vectors and the host (basis of tsetse attraction to the host).
There will be greater progress in epidemiology and epizootiology in the future if identification techniques of trypanosome strains in tsetse and in cattle (DNA probes) are improved as well as models of transmission systems and computerized simulations (Habtemariam et al., 1982-1983a,b).
At the same time efforts must be made to disseminate the knowledge acquired in the field and to gain a better understanding of the real situation of trypanosomiasis in each country.
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