In this chapter the course of the disease, the clinical symptoms, the post-mortem lesions, the pathogenesis (how the disease symptoms and lesions develop) and economical aspects are reviewed.
Trypanosomosis is not one of those diseases that can easily and unequivocally be diagnosed on clinical grounds. In early trypanosomosis departures from the normal state are usually only slight and it is necessary to be keenly observant to appreciate them. People required to diagnose diseases have to be familiar with the various aspects of animals in good health in order to recognize changes from the norm, so that diseases can be diagnosed early and control measures be applied in time.
As far as cattle (taken as an example) are concerned, healthy bovines are bright, alert and aware of their surroundings. Grazing and browsing is followed by resting and ruminating. The eye is bright and clear and the coat smooth and shiny. The ears are held erect, the tail is continually swishing at irritating insects. As a herd animal, the individual bovine is normally rarely seen away from the group for any distance or length of time. The visible mucous membranes of the eye, nostril and vagina are a clear healthy pink colour. Pale mucous membranes indicate anaemia, the most important clinical sign of trypanosomosis, but anaemia occurs in other diseases too, particularly infections with other blood parasites and certain intestinal worms. While the faeces vary to a considerable degree in consistency according to the dryness of the grazing, they normally have a characteristic and inoffensive smell. Dark black or pale yellow or grey liquid faeces with a strong unpleasant odour and the splashing and staining of the hindquarters with liquid matter are always to be regarded with suspicion, although not necessarily related to trypanosomosis. On the other hand, faeces should not consist of very hard balls of material covered with mucus or flecked with blood. The healthy animal keeps its nostrils clean with its tongue, and thick white or yellow discharge should never be apparent. The muzzle should be moist and clean. Breathing at rest should be quiet and regular, at about 10–15 times per minute, but the rate increases greatly when the animal is exposed to the sun in hot weather.
A tendency to sway and stagger indicates weakness or nervous incoordination. The bodily condition is an important indication, both of the individual animal and of the herd. All members of a herd are not usually stricken at the same time by disease, and poor condition of a whole herd, as well as of other herds in the vicinity, may reflect poor seasonal grazing or lack of water, while poor condition of a herd in contrast with others nearby may be a sign of poor management. When poor condition is noticed in some animals only, it is more likely to be caused by disease.
Although rarely taken in the field, the body temperature can be a valuable indication of disease. Normal temperatures of various domestic animals are given in Table 3, but temperatures outside this range should not be regarded immediately as a sign of disease. The body temperature may vary during the course of the day, depending on the ambient temperature. In hot weather and when the animals are excited, the temperature may be well above what is considered to be normal, and be therefore meaningless in such conditions. In particular the camel, adapted to an existence during which there are great variations in the ambient temperature, shows large changes in body temperature, but even in cattle the differences may be surprisingly great. A lack of water, preventing the normal mechanism of heat loss through sweating, may also be responsible for a higher temperature in cattle.
In order to allow for the influence of various factors outlined above, the best time to take the temperature of an animal is in the early morning in rested animals, before the ambient temperature has risen greatly.
Despite these reservations, the temperature is an extremely useful guide to the presence of infectious disease, including trypanosomosis. The animal reacts to an infection by fever; it is a sign of the response of the bodily defences to the invasion by the infective agent. Successful treatment will result in the temperature returning to normal.
On the other hand, an abnormally low body temperature may be taken as a grave sign and can signal approaching death.
In the case of trypanosomosis the temperature fluctuates around an average which is higher than normal. This peaking is caused by antigenic variation (see below).
TABLE 3
Normal temperatures of domestic animals
| Species | °C (upper limit under normal conditions ± 0.5°C) |
| Cattle | 38.5 |
| Sheep | 39.0 |
| Goats | 39.5 |
| Horses | 38.0 |
| Camels | 37.5 (34.5–39.0) |
| Buffaloes (domestic) | 38.3 |
| Pigs | 39.0 |
| Dogs | 39.0 |
In assessing a disease situation the opinion of the herdsmen should not be neglected, because they are continually in the presence of the animals and are best aware of the habits of the individual beasts, of local conditions, seasonal variations and past history. Patient enquiry will often result in the assembly of a great deal of indispensable information. Camel owners may be able to detect T. evansi-infected animals by the smell of their urine. Cattle owners often associate the loss of hair from the tail with chronic trypanosomosis; the author of this field guide does not know whether this association has ever been proved to exist.
Trypanosomosis is a collective term for a group of diseases brought about by one or more of the pathogenic trypanosome species. It should however be remembered that there are differences between infections caused by the various species and strains of trypanosomes in different host species and host populations or breeds, and it must be stressed that there are great differences under the influence of various circumstances.
Typically, trypanosomosis is a wasting disease in which there is a slow progressive loss of condition accompanied by increasing anaemia and weakness to the point of extreme emaciation, collapse and death. However, there is a range of variation from the very acute disease in pigs caused by T. simiae to the usually mild condition caused by T. brucei or T. evansi in cattle. The individual and breed susceptibility are also of utmost importance. Infections that are on the average mild in trypanotolerant West African taurine cattle, such as the N'Dama and the Baoulé, may be severe in susceptible zebu and European taurine breeds.
Animals in good condition and not subjected to physical stress (such as having to transhume or walk far between pastures and waterpoints) usually suffer considerably less than animals on a poor nutritional level and having to expend much physical energy.
In horses extensive subcutaneous oedema is often seen in infections caused by trypanosomes of the subgenus Trypanozoon (T. brucei, T. evansi, T. equiperdum), but also by T. congolense. Infiltration with liquid of subcutaneous tissues may lead in acute T. brucei infections in sheep to swelling of the eyelids, the lips and the skin beneath the lower jaw.
Progressive symptoms of an affection of the central nervous system are not uncommon in horses infected with trypanosomes of the subgenus Trypanozoon; they may show staggering, paralysis, stupor, etc. similar to the symptoms of human sleeping sickness. Small ruminants infected with T. brucei may also show central nervous symptoms.
In the domestic pig, T. simiae produces a hyperacute, fulminating disease, which was described by Sir David Bruce (who first discovered it, and after whom the species T. brucei was named), as “the lightning destroyer of pigs”. After a short incubation period death occurs very rapidly and at post-mortem examination the picture is one of a complete capillary breakdown with haemorrhages and congestion in various organs throughout the carcass. The blood is found to be full of parasites, many sticking together in clumps (agglutination).
In cattle one sometimes encounters a hyperacute haemorrhagic form of trypanosomosis caused by T. vivax, normally a chronic disease. Prior to death animals are bleeding from many sites throughout the body, and at post mortem haemorrhages are very widespread and extensive. The intestinal tract, from the abomasum (fourth stomach) to the rectum, contains large amounts of blood. Large haemorrhages are seen beneath the linings of various organs, the heart, the pleural cavity, the peritoneum, the diaphragm - virtually in every organ and tissue. The disease progresses so quickly to death that there is no loss of condition. If treatment is given in the first few hours, recovery is remarkably rapid. There is a marked fall in the number of platelets in the blood, which play an important part in the process of blood clotting; their numbers are also deficient in some other diseases in which widespread haemorrhages are a feature.
In chronic trypanosomosis the chief pathological factor in the disease is a progressive anaemia with the profound effects this will have on various organs and systems and their basic functions throughout the body. However, anaemia is seen in a whole series of diseases caused by blood parasites (in particular babesiosis and anaplasmosis) as well as certain gastro-intestinal helminths (Haemonchus), and it is therefore not typical of trypanosomosis by itself. (The word anaemia means lack of blood, there is less haemoglobin, the iron-containing protein which transports oxygen to the various organs of the body and gives the blood its red colour.)
The following description would apply to an uncomplicated case of chronic trypanosomosis caused by T. congolense or T. vivax in a susceptible zebu.
The disease becomes apparent about seven to ten days after the infective tsetse bite, when the temperature will rise and the heart and respiratory rates increase. From this point onwards there will be a fluctuating but continuous slow deterioration in health with a steady loss of condition. A typical example of a temperature curve in trypanosomosis is shown in Figure 8.
The animal will become obviously sick with a variable appetite. It tends to leave the herd, seek shade and stand idly with hanging ears and tail, ignoring annoying insects. Its coat becomes dull and “staring” (lacking the sheen associated with good health). There may be some diarrhoea in the early stages.
Loss of condition will soon become obvious as first the fat beneath the skin and then the muscles themselves are greatly reduced and the underlying bones become apparent. The skin often loses its suppleness (“turgor”) because of dehydration, the eyes are sunken and at this stage the classical signs of anaemia are obvious, the visible mucous membranes are pale and the blood is watery in appearance. The emaciation is associated with weakness and in the final stages results in inability to stand, and in pressure sores and ulceration of the skin over the bony prominences.
There is very often an increased secretion of tears (lachrymation). In early acute T. vivax infection in cattle trypanosomes may invade the anterior chamber of the eye, leading to the eye becoming bluish and opaque, and finally blindness may supervene. This condition can be confused with infectious keratitis (inflammation of the cornea) and conjunctivitis. When T. vivax is the cause, trypanocidal treatment leads to a rapid improvement of the eye condition. In dogs T. brucei also attacks the eyes and in this case in addition haemorrhages into the anterior chamber of the eyeball can result in blindness which will not respond to treatment.
The usefulness of a post-mortem (PM) examination depends upon a basic knowledge of what is normal; this can only be obtained by practical experience, especially under the guidance of an experienced and skilled operator who can demonstrate PM techniques and pathological changes. Inspecting carcasses in an abattoir can be extremely useful, as long as one remembers that such carcasses have been bled, and the appearance of some organs therefore can be very different from those of animals which have died from other causes. For example, the lungs after slaughter and bleeding present an altogether different appearance from those of an animal which has died in a different way.
The PM findings in trypanosomosis can never by themselves lead to a certain diagnosis of the cause of death. There is not one single specific lesion.
In the acute stage there is loss of condition and anaemia, but not as severe as in chronic trypanosomosis. Miscroscopic examination of the blood will show that the haemopoietic system is actively trying to compensate for the loss of red cells (regenerative changes such as anisocytosis, normoblasts, Howel-Jolly bodies, basophilic punctations). The spleen is enlarged. The lymph nodes are enlarged and oedematous (containing more liquid than usual). The liver is enlarged and congested. The heart may be somewhat enlarged and may show a few haemorrhages on the muscle surface. There is also likely to be more fluid than normal in the chest, lungs, abdomen and pericardium (heart sac). The kidneys are pale and swollen. Subcutaneous oedemas may be present particularly in horses and sheep.
In chronic trypanosomosis the pathological changes seen at post mortem are more striking, without being typical. The carcass is emaciated and often dehydrated. The skin may show pressure sores and ulcers, when the animal has been unable to stand up for some time. The fat reserves under the skin have been used up and the skin is closely adherent to the underlying muscles and bone. The muscles have wasted to a remarkable degree and the underlying bones are prominent. The muscles are pale because of the anaemia and the blood is watery and pale, with an increased clotting time. The heart is often enlarged and flabby because of muscle deterioration, and its weaker pumping action may have contributed to circulatory disturbances and increased fluid in the tissues (oedema). Unlike the picture seen in acute trypanosomosis, the lymph nodes are mostly normal or even hard, dry and reduced in size. The spleen is also normal in size or contracted with a drier pulp than normally seen.
When the tsetse fly injects infective metacyclic trypanosomes into the skin of the host, there is a phase of local inflammation and a swelling, a so-called chancre, develops. The metatrypanosomes divide and multiply in the chancre and give rise to the typical blood forms which invade the lymphatics and lymph nodes, and then the blood stream.
Trypanosomosis, like other infectious diseases, starts with an increase of the body temperature, a hyperthermia. This is the result of the contact between the trypanosomes multiplying in the host and the defence system of the host. The surface proteins of the trypanosomes provoke the host in making specific antibodies against these proteins, and after a few days almost all of the trypanosomes in the blood are destroyed by these antibodies and the body temperature drops. However, a few parasites survive as they have been able to replace their surface proteins by different ones, against which the antibodies cannot act. These surviving trypanosomes are able to multiply, and cause a new peak of parasitaemia and hyperthermia, until the organism of the host makes specific antibodies against the new surface proteins. This seesawing process continues for a long time, as the trypanosome is able to make an almost unlimited number of antigenic variants, and the host responds to each of them, until either the antigenic repertoire of the trypanosome is finally exhausted, in which case self-cure of the host follows, or the ability of the host to react to all of the antigenic variants is overwhelmed, and the host dies.
A typical aspect of trypanosomosis therefore is the temperature curve: there are peaks every few days, particularly in the beginning. Antigenic variation becomes slower as the disease progresses and the intervals between temperature peaks become longer and the peaks are less high. Figure 8 illustrates this.
Figure 8
Temperature curve in a bovine suffering from T. congolense infection
One of the main symptoms of the disease is anaemia (decrease of haemoglobin in the blood). There are various theories on the pathogenesis of anaemia. In the early stages of the disease, it is believed to be caused in part by phagocytosis of red cells (their removal by a certain type of the host's white cells, the phagocytes). The red cells apparently become coated with material from lysed trypanosomes which tricks the phagocytes into mistaking them for foreign invaders and remove them. (This phenomenon is also called auto-immunity = immunity directed against cells of the host itself.) It is possible that the anaemia caused by phagocytosis is increased by toxic substances emanating from the trypanosomes which destroy red cells directly by lysis (haemolysis). The haemopoietic system (the system which produces red cells, mainly in the red bone marrow), tries to compensate for the loss of erythrocytes by increasing its activity but, later, in the chronic stages of trypanosomosis, othertoxins from the parasites have a depressing effect on the haemopoietic system, and the host is unable to produce as many red cells as are removed (even normally these cells have only a limited life span, and now they are removed even faster because of auto-immunity and haemolysis).
The anaemia means a reduction in haemoglobin and therefore in the oxygen-carrying capacity of the blood. Insufficient oxygen is available to the cells for their efficient functioning and the efficiency of their normal activities is reduced. A slow process of deterioration of health and condition sets in.
Trypanosomosis is also associated with immunodepression,19 i.e. the host's immune system becomes less efficient to deal with infections. Although this can perhaps be explained in part by the depression of the haemopoietic system, which not only provides red cells but also white ones involved in the immune response, immunodepression occurs also in the acute stage; the ability of the immune system to react to invaders is already diminished before the haemopoietic system is depressed. Animals affected by trypanosomosis often develop a lower antibody titre after vaccination against other diseases, and secondary infections which the host would normally control may also crop up during the disease. For example it is common to find considerable numbers of Babesia, Theileria and/or Anaplasma in bloodsmears of animals suffering from AAT, in situations where normal animals are healthy carriers of these tickborne infections. Trypanosome infections disrupt the balance. Such concurrent diseases may also affect necropsy findings.
Various organs are affected by AAT, to some extent depending on the species involved. While (more or less hypothetical) toxins may be involved, as well as the anaemia (see above), the trypanosomes may also be more directly responsible. T. congolense is mainly confined to the blood, while T. vivax and T. brucei also invade the tissues. T. vivax is found in the lymph and even in the chamber of the eye and T. brucei is well known to invade the central nervous sytem in human sleeping sickness (T. brucei gambiense and T. brucei rhodesiense), but also in animals such as horses, goats and dogs. The nervous system is also affected in the later stages of dourine (T. equiperduni).
The heart is often affected by a myocarditis (inflammation of the heart muscle), and heart failure is often the direct cause of death. However, this depends to a large degree on the effort the heart muscle has to provide. Extensive myocarditis with the presence of trypanosomes in the heart muscle has been found in highly susceptible European cattle infected experimentally in Europe with pathogenic West African T. vivax, kept at rest in a stable and on a good level of nutrition, and which had shown no obvious signs of distress before they were slaughtered at the end of the experiment. Such infections could easily have caused fatal heart failure in African zebu cattle subjected to the stress of poor nutrition and walking long distances to watering points or during transhumance.
Oedemas (subcutaneous swellings caused by accumulation of tissue fluid) are often present in trypanosomosis, particularly in horses and dogs. There is evidence of increased permeability of blood capillaries, and therefore leakage of blood plasma leading to the swellings.
In chronic trypanosomosis the animal loses condition, there is wasting. During the acute stage, the appetite is variable, being decreased during the fever peaks. But in the chronic stage, when the fever reactions are less pronounced, the appetite is usually normal, almost until death, even when extreme weakness prevents the animal from rising. The pronounced wasting is therefore not caused by starvation. There is consumption of the fat reserves during the recurrent bouts of fever, but there are also severe degenerative changes of the muscle cells and other tissue cells, and there is an increased breakdown of protein in muscles and elsewhere, leading to atrophic degeneration (the cells are reduced in size and efficiency). The decreased supply of oxygen because of the anaemia is also an important factor (see above).
In high challenge areas, and in the absence of trypanotolerant breeds, tsetse flies and AAT prevent the keeping of livestock, at least of those species that are affected by AAT. In that case, the economic impact on livestock production is most pronounced. In several African countries livestock (draught oxen) and their products (manure) play an important role in crop production, and the integration of livestock in crop agriculture is therefore severely affected.
Keeping non-susceptible livestock, in particular poultry, may be the best answer to solving the problem of providing sufficient animal proteins in the human diet. Or game farming may be a feasible option. Sometimes the area is more suitable for the production of valuable agricultural crops which can be sold and the income used to buy animal products from elsewhere.
All kinds of situations exist between this extreme case and the absence of trypanosomosis; the economic impact varies accordingly. Many factors are involved when economic aspects are considered, such as:
The economic impact is made up of direct losses (consisting of loss of production, mortality, abortion), as well as the cost of control (which includes the cost of drugs, their transport to the field site, the salaries of the operators, etc.).
The loss of potential production (i.e. the production that could be achieved if trypanosomosis did not occur) are indirect losses. At present unused grazing areas in many of the tsetse-infested areas of Africa could support a large ruminant livestock population. However, the control of the fly should only be envisaged when really needed, and then only when proper and sustainable land-use plans have been elaborated, and when the political will and legislative means to carry such plans through are assured. If not, overgrazing is bound to occur, followed by erosion and, depending on the climatic zone, by desertification, leading to permanent loss of the land. In the meantime, the presence of tsetse fly preserves these areas.
Because livestock keepers avoid certain tsetse-infested areas, cattle distribution is often imbalanced or even distorted. From the continental cattle distribution we know that this indirect effect of AAT is very important; only 10 million out of 165 million head of cattle in the tsetse-infested countries of sub-Saharan Africa are distributed within the limits of the continental fly belt while most of the remainder is distributed at the perimeter of the fly distribution. At the local level, it is extremely difficult to clarify this point because nobody is sure about the magnitude of these indirect losses. Still, the collective, indirect AAT losses are estimated by FAO to be in excess of the 0.6 to 1.2 hundred thousand US dollar direct losses incurred by trypanosomosis-affected cattle.
Increasingly, tsetse and trypanosomosis control schemes become concentrated in selected areas of high priority. These are areas where control is technically feasible, where the economic returns are considerable and where the transformation of the landscape, from bush to farmland, already occurs because of demographic pressure. It is in such dynamic environments, which become progressively less suited for tsetse survival, that it is economically attractive to intervene.
It is important to monitor the changes during such interventions. Data have to be collected to check on what happens to tsetse-transmitted trypanosomosis, how farming practices and the landscape change. Close monitoring makes it possible to adjust control programmes for technical reasons, or make the programme more efficient in agricultural (economical) terms, or adapt to environmental degradation risks.
Simulation models are useful to examine the economic impact and to decide upon suitable control strategies to achieve a positive cost-benefit result, taking into account the range of various parameters in any particular situation (see, for example, Brandl, 1988). Because of the land-use aspects, there is a growing tendency towards the collection of georeferenced data, which may be plotted on maps; computerized versions may be examined in the so-called geographical information systems (GIS).
Studies on T. vivax and T. evansi in Latin America show that their economic impact can be quite severe. Trypanosomosis of domestic animals has been ranked as third in importance in Colombia, after ticks/tickborne diseases and liver fluke. Even the inapparent losses of subclinical infections by T. vivax may be considerable and the same certainly applies to mechanically transmitted trypanosomosis in Africa; futher economic studies are necessary in order to obtain reliable figures.
