Insects are usually involved in the natural transmission of the African pathogenic trypanosomes with which we are concerned in this field guide. When this is the case, the life cycle has two phases, one in the insect vector and one in the mammalian host. Transmission by insects may be cyclical by tsetse flies,3 Glossina species, or mechanical by other biting flies (but apart from transmitting trypanosomes cyclically, tsetse flies can also act as mechanical vectors).
3 We assume that the reader has some knowledge of tsetse flies, as there simply is no scope in this manual for going into details. At present 23 different species and eight subspecies of the genus Glossina are recognized, belonging to three groups: fusca group or forest group, palpalis group or riverine group, and morsitans group or savannah group.
When a tsetse fly hatches from its pupal case it is free from trypanosomes. Until its first bloodmeal, it is called a teneral fly. It acquires a trypanosomal infection when feeding on a parasitaemic (= having parasites in the circulating blood) mammalian host. The trypanosomes undergo a cycle of development and multiplication in the digestive tract of the fly until the infective metacyclic trypanosomes (metatrypanosomes) are produced. As indicated in Table 1 (p. 32), different trypanosome species develop in different regions of the digestive tract of the fly, and the metatrypanosomes occur either in the biting mouthparts or the salivary glands. The period from ingesting infected blood to the appearance of these infective forms varies from one to three weeks; once infective metatrypanosomes are present the fly remains infective for the remainder of its life. During the act of feeding the fly penetrates the skin with its proboscis. By the rupture of small blood vessels a pool of blood is formed in the tissues and the fly injects saliva to prevent coagulation. Infection of the host takes place at this stage, with infective metacyclic trypanosomes in the saliva.
Although no classical sexual processes in the life cycle of trypanosomes have been described, it has been shown that exchange of genomic material (DNA) between trypanosomes sometimes occurs in the tsetse fly, although it is not clear how significant this is.
Life cycle in the mammalian host. The infective metatrypanosomes undergo development and multiplication at the site of infection where a swelling or chancre may be detected in the skin, and finally the mature blood trypanosomes (or trypomastigotes) are released via lymph vessels and lymph nodes into the blood circulation.
Reproduction in the mammalian host occurs through a process of binary division, details of which are described in Morphology, p. 14.
Trypanosomes feed by absorbing nutrients, through their outer membrane, from the body fluids of the host. The proteins, carbohydrates and fats are digested by enzyme systems within their protoplasm. Oxygen dissolved in the tissue fluids or blood plasma of their host is absorbed in a similar manner, to generate the energy necessary for the vital processes.
Waste products are disposed of by a reverse process, through the outer membrane, into the body fluids of the host. They include carbon dioxide formed during respiration, as well as more complex metabolic products.
Life cycle in the tsetse fly. The site of the different trypanosome species in the fly is indicated in Table 1. Blood stream forms (trypomastigotes) ingested by the fly undergo considerable changes, in morphology as well as in their metabolism. They change into long slender forms called epimastigotes, which multiply and finally give rise to the infective metatrypanosomes. For a detailed account of the different forms and the development in the tsetse fly, the reader is referred to standard text books (see Further reading on p. 157).
By biting insects. The process is purely mechanical. A biting insect passes the blood forms from an infected animal to another in the course of interrupted feeding. The time between the two feeds is crucial for effective transmission because the trypanosomes die when the blood dries. The importance of this mode of transmission is variable from place to place, depending on the numbers of hosts and biting insects present, and also on the species of trypanosome. Large biting insects such as tabanids carry more blood and are more likely to act as mechanical vectors than for example mosquitoes. (Tsetse flies themselves can of course also act as mechanical vectors.) This mode of transmission has proved to be sufficiently effective to maintain Trypanosoma vivax and Trypanosoma evansi in South and Central America, and the latter species in North Africa and Asia as well. No tsetse flies occur outside tropical Africa, apart from small tsetse pockets in the southwest of the Arabian peninsula.
By iatrogenic4 means. This can occur when using the same needle or surgical instrument on more than one animal, at sufficiently short intervals that the blood on the needle or instrument does not dry. It is not an uncommon occurrence when animals are vaccinated or treated by injection, or when blood is collected from several animals in a row, without changing or disinfecting needles or pins. It may also occur when several animals are subjected at short intervals to a surgical intervention (dehorning, castration, etc.) without properly disinfecting the instruments.
4 Iatrogenic transmission means that it is caused by the (veterinary) operator. Iatrogenic infections are induced (involuntarily) by the operator using unhygienic procedures, such as contaminated instruments.
A sound knowledge of the basic features of the various trypanosomes enables the identification of each species and so the exact cause of the disease. Once the basic features possessed by all trypanosomes are appreciated, the diagnostic differences can be recognized and the species identified.
Figure 1 is a diagrammatic illustration of the fundamental features of a trypanosome (trypomastigote) as seen in a stained preparation made from the blood of an infected animal.
Diagram of a trypanosome
The parasite consists of a single cell varying in size from 8 to over 50 μm.5 All the activities associated with a living organism take place within this unicellular organism — nutrition, respiration, excretion, reproduction. The substance of which all living cells consist, the protoplasm, comprises three parts, an outer protective and retaining layer, the pellicle = cell envelope = cell membrane, within which the cytoplasm forms the bulk of the contents. Suspended in the cytoplasm are various structures, the most prominent being the nucleus, which may be regarded as the command centre of the cell and which also plays a major part in reproduction. It contains DNA (deoxyribonucleic acid), which is arranged in the form of genes and chromosomes; it represents the genetic information and is responsible for the manufacture of enzymes and other proteins of the cell.
Small granules (formerly called “volutin granules”) can sometimes be seen in the cytoplasm; they may have various origins, they may be food or nuclear reserves, or result from a reaction between the trypanosome and the host's immune system.
Trypanosomes are thoroughly adapted to living and moving in the blood plasma or tissue fluid of the host. They are elongated and streamlined, and tapered at both ends. The pellicle, the outer layer of the cytoplasm, is flexible enough to permit a degree of body movement, while retaining a definite shape. As shown in Figure 1, a flagellum arises near to the posterior end from a parabasal body, and runs the length of the trypanosome; it may be continued beyond the anterior end of the body as a whip-like free flagellum. Along the length of the body the pellicle and cytoplasm are pinched up into a thin sheet of tissue called the undulating membrane, through the outer margin of which runs the flagellum, as shown in Figure 1.
Among other basic morphological features, a distinct well-defined body, the kinetoplast, is seen near to the posterior end of the trypanosome and differs in size and position according to the species. It is adjacent to the parabasal body (from which the flagellum arises), and so close to it that it cannot easily be seen separately with the light microscope. The kinetoplast has important functions in reproduction and metabolism and is probably essential for cyclical transmission by tsetse flies. (It is sometimes absent in a proportion of.trypanosomes, especially of some strains of T. evansi, a species which has lost its ability of being cyclically transmitted.) The extent of the undulating membrane and the absence or presence of the free flagellum are also precious in specific identification of trypanosomes. Other morphological characters are the average length and the shape of the body.
5 One μm is a micron, a millionth of a metre or a thousandth of a millimetre.
Trypanosomes move actively and progress by movement of the undulating membrane and the free flagellum (when present), which acts as a kind of propeller, thus drawing themselves through the blood plasma or tissue fluid. (The free flagellum, when present, arises from the anterior [front] end of the parasite.) The movement pattern as seen with the microscope in fresh blood preparation can be of some help in identifying the species involved, particular for Trypanosoma vivax, which moves rapidly forward between the blood cells, whereas other species often just wriggle around without showing much forward progress.
This is by a process of division to produce two daughter cells. However, as stated above, it has been shown that exchange and recombination of genetic material may take place in the tsetse fly between two trypanosomes, but it is unknown how frequently this occurs.
The division into two daughter cells (binary fission) follows the sequence of events illustrated in Figure 2. The kinetoplast divides first. A second parabasal body develops, from which a second flagellum develops. The nucleus divides next, followed by the rest of the trypanosome body duplicating all the structures present in the cytoplasm. The body then divides into two daughter cells, beginning at the anterior end. The process is rapid, and may result in a vast population in the host within a short period of time.
Division of a trypanosome
There are distinct differences in appearance, shape and size between the various species of trypanosomes, allowing specific identification. It must be remembered, however, that in any biological material there is some variability. Also, trypanosomes are not rigid and continuously change their shape slightly; the individual parasite seen in the stained preparation presents the shape it had at the moment of dying. It has also been subjected to the unnatural stresses of drying out and being fixed and stained. Many variations in appearance are therefore seen, differing somewhat from the drawings in textbooks. It is thus necessary to observe carefully and systematically all the features in a sufficiently large number of individual trypanosomes; only after such an examination is it possible to arrive at a reasonably accurate diagnosis. There will be examples where trypanosomes are so few, or the staining so inadequate, that identification may not be possible or only after a prolonged search. It is also essential to examine several individual trypanosomes, because even if one specimen is sufficiently perfect to establish its identity beyond any doubt, further search may reveal another species and thus a mixed infection. Mixed infections occur more often in the field than was previously thought, as new more sensitive diagnostic techniques have shown (see Chapter 3 - Diagnosis).
For specific identification, a number of trypanosomes should be examined systematically for the presence or absence, size and position of a number of features:
It is important to remember that the successful use of this simple key depends on the presence in the preparation of a sufficient number of individual parasites. It is not always possible to make an accurate diagnosis if only one or two parasites can be found after a prolonged search. The task is rendered more difficult or even impossible if the stained preparation is of poor quality.
Taxonomy is the classification and orderly arrangement of living organisms according to their structure and shape (morphology), their biological development (life cycles) and, more recently, their molecular structure, particularly that of their genome (molecular taxonomy). Nomenclature, the system of naming organisms, is based on their classification. Without going into great detail, let it be recalled that organisms are classified into large divisions called phyla (singular phylum), then into classes, orders and families. For example, the Diptera are an order of the class of insects, which belongs to the phylum of the arthropods, and the Glossinidae or tsetse flies are a family of the Diptera. The family Trypanosomatidae (which includes trypanosomes, but also for instance leishmanias) belongs to the order of the Kinetoplastida, the class Zoomastigophorea and the phylum Protozoa. Each species is furthermore given two names, the first, always spelled with a capital letter, places it in a relatively small group known as the genus (plural genera) and the last name, spelled with a small letter, indicates the species. The family Glossinidae comprises only one genus, Glossina, which includes over 20 species of tsetse flies. Sometimes a genus is subdivided into subgenera, and an additional name is sometimes added to denote a subspecies, when differences within one genus and/or species are so wide that a further breakdown is helpful (e.g. Trypanosoma [Trypanozoon] brucei gambiense, which is the causal agent of classical human sleeping sickness; details of this name will be explained a little further on). The genus (or subgenus), species (or subspecies) may be further defined by adding the surname of the person who first described it and the year when the description was published (e.g. Trypanosoma congolense Broden, 1904 indicates that Broden in 1904 published the first description of this important pathogenic trypanosome of cattle in tropical Africa).
Another subdivision of the genus Trypanosoma, into two sections, is mainly based on the way in which the infective forms leave the intermediate insect host after their cyclical development.
In the section Stercoraria, development in the vector ends with the formation of infective metatrypanosomes in the posterior part of the digestive tract and transmission occurs through the faeces of the insect,6 while in the Salivaria, with which we are mainly concerned in this field guide, the usual mode of transmission is inoculative, through the biting mouthparts of the vector (except for dourine).
In higher organisms a species is defined as a group of organisms that can interbreed with one another to produce fertile offspring. In the case of viruses, bacteria, and many of the protozoa, where no (classical) sexual processes are known to occur, the definition of species is more arbitrary and some scientists adhere to the principle that a valid species is one that is recognized by a good taxonomist. In addition to morphological and biological characteristics, molecular taxonomy is now increasingly used.
Once the identity of an organism has been stated in a scientific paper or book, it is customary to shorten the genus name to its initial capital letter and omit the name and year of the person who first described it (e.g. Trypanosoma congolense Broden, 1904 becomes T. congolense.)
6 The Stercoraria include for example the species Trypanosoma cruzi, which causes human trypanosomosis in Central and South America, also called Chagas disease; although it may be of even greater importance as a human disease than African sleeping sickness, it has fortunately no economic impact on livestock production.
Trypanosomes are unicellular organisms (Phylum Protozoa) belonging to the genus Trypanosoma, the family Trypanosomatidae and the order Kinetoplastida. Many species of trypanosomes occur as parasites in a wide variety of animals, and even plants. For the purpose of this field guide we are concerned with those causing disease (the pathogenic trypanosomes) in domestic animals in Africa (African animal trypanosomosis = AAT). Some of these parasites have been spread by humans from Africa to other continents. For example, T. vivax had been introduced to the Americas, by the importation of West African cattle in the eighteenth and nineteenth centuries, and it is likely that T. evansi had already “escaped” from Africa far earlier by animal movements (in particular camels) between Africa and Asia.
Trypanosomes are blood parasites (haemoparasites), from the word haem = blood, which in the vertebrate host occur in the blood and tissue fluid and within that group are known as haemoflagellates, as they progress actively by the movement of the thread-like filament called flagellum.
The trypanosomes causing AAT belong to three subgenera, as shown in Table 1.7
7 A fourth subgenus, Pycnomonas, which comprises one species, T. suis, is a rare and poorly known parasite of pigs (and wild pigs such as wart hog), which we shall not mention any further.
The subgenus Nannomonas (the congolense group). T. congolense (see Figure 3). This is the smallest of the pathogenic trypanosomes, with a length of 9–22 μm.
Trypanosoma congolense as seen in a stained blood smear
The blood forms are monomorphic, in that they lack a free flagellum (in the longer forms the shape of the anterior extremity may suggest the presence of a very short free flagellum). The use of the term monomorphic is somewhat misleading in this species in that there is a variation in size and shape between strains. Generally two variants are to be seen, a shorter form (9–18μ), the typical congolense type and a longer form (up to 25μ), with individuals intermediate in length between the two. The proportion of long and short forms varies in different cases and, it has been said, localities of origin. There is evidence which indicates that strains with the most long forms, the so-called “dimorphic” strains, cause a more severe form of trypanosomosis.
Recent studies have now resulted in a subdivision of the species in several “types”, which can be distinguished by isoenzymatic differences8 and molecular techniques.9 Only one type has received a separate species name, T. godfreyi (see below), as it is also different in its pathogenicity for various hosts, while the others are designated as T. congolense savannah type, T. congolense Tsavo type, T. congolense forest type, T. congolense Kilifi type. For the purpose of this practical field manual we shall use only the name of T. congolense for these four types, but it should be remembered that from a scientific point of view this name encompasses rather different parasites and possibly more than one species.
In stained specimens of T. congolense the cytoplasm stains a diffuse, even, pinkish colour and is seldom granular.
The nucleus is centrally placed. The kinetoplast is of medium size and is usually situated at the margin of the body, just in front of the posterior extremity (marginal and subterminal).
The undulating membrane is poorly developed and inconspicuous.
T. simiae (see Figure 4). Trypanosomes of this species are polymorphic, with a length of 12–24 μm. In typical cases some individuals are with and others without a free flagellum.
8 Isoenzymes may be defined as enzymes which have identical functions but show molecular differences that can be detected with appropriate techniques.
9 Such as those mentioned in Chapter 3 on diagnosis under molecular tests (DNA probes, PCR).
Trypanosoma simiae blood stream forms
The kinetoplast is of medium size, marginal and subterminal, as in T. congolense. Three morphological types can be recognized:
T. godfreyi. This species has been separated recently from T. congolense in the Gambia, on the basis of isoenzymatic and DNA differences, but also because the disease it causes is different. It is pathogenic for pigs, but the disease is more chronic than the one caused by T. simiae. Morphologically it is similar to T. congolense, with a length of 9–22 μm (mean 13.7), but the undulating membrane is described as being usually conspicuous.
The wart hog appears to be its normal host and constitutes a reservoir of infection for domestic pigs.
The subgenus Duttonella (the vivax group). T. vivax (see Figure 5). This trypanosome as seen in the blood of mammals is also essentially monomorphic, with a free flagellum. Its length, including the free flagellum, varies from 18 to at least 26 μm. The following description concerns typical specimens.
The kinetoplast is large and terminal or almost so. It is much larger than in any of the other pathogenic species, and this is a distinguishing feature.
The nucleus is centrally placed, but the bulk of the cytoplasm is found in the posterior part of the body as this is somewhat swollen.
The posterior extremity is swollen and blunt.
Trypanosoma vivax blood stream forms
The undulating membrane is inconspicuous.
A more slender form is sometimes seen, which possesses a more pointed posterior extremity and has been thought to cause a more severe form of the disease. Such forms are commonly seen when T. vivax is dividing rapidly in the blood and it has also been reported that T. vivax in Latin America is more slender than the typical African parasite.
T. uniforme. Small trypanosomes (from 12 to 20 μm), otherwise similar to T. vivax, have been given the name T. uniforme. It is not recognized as a separate species by all specialists; some regard it as a subspecies (T. vivax uniforme).
The subgenus Trypanozoon (the brucei group). This group comprises five members: T. brucei brucei, T. brucei gambiense, T. brucei rhodesiense, T. evansi and T. equiperdum. The three subspecies of T. brucei are normally transmitted by tsetse flies (in contrast to T. evansi and T. equiperdum) and are exactly similar in morphology, but only T. brucei gambiense and T. brucei rhodesiense are the cause of human sleeping sickness, the former mainly in West and Central Africa and the latter in eastern and southern Africa. T. brucei brucei is not infective to humans.
T. brucei (see Figure 6). T. brucei is polymorphic, with three main forms, all of which have a small kinetoplast and a conspicuous undulating membrane:
Trypanosoma brucei blood stream forms
During the course of the infection, there is a change in the trypanosome population from the long thin forms, through the intermediate, to the short stumpy, and this altered appearance is accompanied by a change in the type of respiration, as the trypanosome prepares for its period within the tsetse fly. The short stumpy forms are adapted to living and developing in the tsetse, while long thin forms are the true mature blood forms which die in the gut of the insect. (Similar metabolic changes also occur in other trypanosome species, but there are no such obvious morphological changes associated with them as in T. brucei.)
As noted above, the species T. brucei is subdivided into three subspecies, T. brucei brucei, African trypanosome transmitted by tsetse flies, not infective to humans, T. brucei gambiense, the causal agent of classical or Gambian human sleeping sickness, and T. brucei rhodesiense, which causes the type of human sleeping sickness common in Zimbabwe.
T. evansi.10 T. evansi cannot be distinguished on morphological grounds from the long slender forms of T. brucei, and it is almost certain that T. evansi has developed from T. brucei by continual mechanical passage (particularly through camels), the vectors being blood-sucking flies, especially those of the Tabanid family. The disease, often called surra in Asia and by a variety of names elsewhere, such as el debab (northern Africa), mal de caderas (Brazil), murrina (Central America), has spread over a wide area outside the tsetse belts in Africa, in the Near East, India, China and Southeast Asia, as well as in tropical America. Direct mechanical transmission has resulted in T. evansi losing its ability to undergo the developmental cycle in tsetse flies.
Its length is from 17 to at least 30 μm, and the description given for the long slender forms of T. brucei fits T. evansi. Nevertheless, short stumpy and intermediate forms may be seen rarely, irregularly and in very small numbers, including posteronuclear forms. A greatly varying proportion of individual trypanosomes may have no visible kinetoplast and there are even strains of T. evansi in which the kinetoplast is not apparent in any individual trypanosome, the so-called akinetoplastic strains (such strains have in the past been considered in Latin America as a separate species, T. equinum, but this name is no longer considered valid).
T. equiperdum. This is another trypanosome which is probably derived from T. brucei. Its morphology is identical to that of T. evansi and the long slender forms of T. brucei, but it is different in that it causes a natural disease only in animals of the horse family (horse, donkey, mule), among which it is transmitted by genital contact. The disease, dourine, is thus a venereal disease. As it is not dependent on insect vectors, it has spread as far north as Canada, Russia and other European countries, and as far south as Chile and South Africa. (It has since been eradicated in many countries.)
10 Because this trypanosome is believed to be derived from T. brucei brucei, the name T. brucei evansi is sometimes used for it. Nevertheless, this particular trinomial name is invalid according to the rules of the international code for zoological nomenclature, as the name evansi was created before the name brucei. In order not to cause confusion, we will stick to using the commonly accepted species names of T. brucei and T. evansi.
T. theileri and other species of the subgenus Megatrypanum (Stercoraria). T. theileri in cattle, domestic buffalo and various wild Bovidae (members of the family of bovines), and also related species such as T. ingens (antelopes and cattle), are normally non-pathogenic and only concern us because they can confuse the parasitological diagnosis of trypanosomosis. T. theileri is a cosmopolitan species (occurring all over the world), transmitted by tabanid flies and probably also by ticks. It is a large species (from some 30 to over 60, even 100 μm), normally very scanty in the peripheral blood, but it is encountered relatively frequently by careful observers. Its large size and its morphology are distinctive features. In stained smears it cannot be confused with the pathogenic species, because of its large size, the position of the kinetoplast (far from the posterior extremity), and its finely pointed posterior extremity. Even in the buffy coat, its large size and sluggish movements often allow the diagnosis of Megatrypanum sp. Of the other species of Megatrypanum only T. ingens is also sometimes found in cattle; it is also an unmistakable huge trypanosome, deeply staining with Giemsa, and with a typical band-like transverse nucleus. (Non-pathogenic species of Megatrypanum also occur in sheep and goats, but they are so seldom encountered in blood preparations that we will not discuss them.)
Classification of the pathogenic African trypanosomes11
|Duttonella||Vivax group:||In tsetse: proboscis only|
|T. vivax||Can also persist by mechanical transmission|
|Nannomonas||Congolense group:||In tsetse: midgut and proboscis|
|T. congolense||Not known to maintain itself exclusively by mechanical transmission|
|Trypanozoon||Brucei group:||In tsetse: midgut and salivary glands|
|T. brucei brucei|
|T. brucei rhodesiense **||Oral transmission in carnivores|
|T. brucei gambiense **|
|T. equiperdum||Mechanical transmission12|
* Congenital transmission is not mentioned in the table but, in principle, any species may occasionally be transmitted in this way.
** Causal agents of human sleeping sickness.
11 As noted in the text, recent studies, using modem molecular techniques, have shown that there are more types/species within each group than indicated in this table. So far, most of these types have not been given separate species names. In the absence of a clear vision of what constitutes a species in micro-organisms in which the rules for higher organisms do not easily apply, we will stick to the old nomenclature.
12 Oral transmission in carnivores and vampire bats.
Table 2 indicates the occurrence of the pathogenic African trypanosomes in common domestic animals. Also included are the two non-pathogenic species of theileri group mentioned above, which may give rise to confusion; they belong to the subgenus Megatrypanum and the section Stercoraria.
Within each species there is a great variety of strains which may be classified in a number of ways. One way of classification is according to the pathogenicity, virulence, or disease-producing potential of the strain, and this can be extremely variable. The course and outcome of trypanosomosis is in addition influenced by a whole range of coexisting factors and influences, which combine and react to exert profound effects. No attempt therefore has been made to include a column in Table 2 summarizing the severity of the disease produced in each animal species by each trypanosome species. Such an attempt would be meaningless and misleading. The only indication of pathogenicity in Table 2 is that in the second column the list of livestock species is tentatively ranked in descending order of importance. In the fourth column the susceptibility of the common laboratory animals is indicated, which can be of some importance in certain diagnostic procedures, as will be seen in Chapter 4.
The occurrence of African trypanosomes in domestic animals
|Trypanosome species||Domestic animals affected||Reservoir hosts||Laboratory animals|
|T. congolense||Cattle, camels*, horses, dogs, sheep, goats, pigs||Several groups of wild mammals||Rats, mice, guinea pigs, rabbits|
|T. simiae||Pigs||Wart hog, bush pig||Rabbits, monkeys|
|T. godfreyi||Pigs||Wart hog||None susceptible|
|T. vivax||Cattle, sheep, goats, domestic buffalo, horses||Several groups of wild mammals||Usually none susceptible|
|T. uniforme||Cattle, sheep, goats||Various wild ruminants||None susceptible|
|T. brucei brucei||Horses, camels*, dogs, sheep, goats, cattle, pigs||Several groups of wild mammals||Rats, mice, guinea pigs, rabbits|
|T. brucei gambiense,|
T. brucei rhodesiense
|Human sleeping sickness; affect domestic animals as T. brucei brucei**||Several groups of wild mammals (particularly T. brucei rhodesiense)||As for T. brucei brucei (after initial adaptation where T. brucei gambiense is concerned)|
|T. evansi||Camels, horses, dogs, domestic buffalo, cattle||Several wild mammals in Latin America||As for T. brucei brucei|
|T. equiperdum||Horses, donkeys, mules||None known||As for T. brucei brucei (after initial adaptation)|
|T. theileri and T. ingens (subgenus Megatrypanum)||Cattle, domestic buffalo*** (not pathogenic)||Various wild ruminants||None|
* Camels are highly susceptible to T. congolense and to T. brucei, but do not usually penetrate into tsetse country.
** In particular, the behaviour of T. brucei rhodesiense in domestic animals is quite similar to that of T. b. brucei, whereas T. brucei gambiense is on the average more chronic (as it is in humans).
*** Of the two only T. theileri has been reported from domestic buffalo.
So many factors intervene in the epidemiology of African trypanosomosis that an entire book could be written on the subject. In the context of this guide we cannot possibly discuss all the possible scenarios and have to restrict ourselves to the main factors.
For general principles of epidemiology, we refer to books such as those by Putt et al. (1986) and Martin, Meek and Willeburg (1987). It is essential to be familiar with the fundamental terms used in epidemiology, for example, the difference between prevalence and incidence. It is also essential to distinguish between disease as opposed to infection; particularly trypanotolerant animals may be infected without having clinical disease, in other words, they may be healthy carriers. Prevalence is the frequency of existing cases of disease, or of infection, at a certain time. Incidence indicates the frequence of new cases within a certain period of time. Where it is possible to determine prevalence and incidence by certain tests, it is important to use a correct sample size, and for those with some statistical background considerations on sample size have been included at the end of this manual.
One all-important factor is whether we are dealing with tsetse-transmitted trypanosomosis or not. If so, much depends on the Glossina species responsible for transmission. There is a large body of experimental evidence to show that host preferences and vector capacity differ greatly between groups and species of Glossina. For example, recent laboratory experiments with teneral tsetse flies in Burkina Faso have shown higher mature infection rates with the savannah type of T. congolense in G. morsitans morsitans14 and G. morsitans submorsitans (both belonging to the savannah group of tsetse) than in G. palpalis gambiensis and G. tachinoides (palpalis or riverine group). G. morsitans submorsitans was the best vector of both the savannah and the riverine-forest types of T. congolense, while G. m. morsitans had the lowest vectorial capacity for the riverine-forest type; G. palpalis gambiensis was the least effective vector for the savannah type of T. congolense.
Savannah species are on the whole better vectors of the pathogenic trypanosomes of livestock. Also, where savannah tsetse (morsitans group) are the vectors, the risk of contracting the disease is widespread, although their distribution area in the dry season decreases. When riverine species are the culprits (in many parts of West and Central Africa), transmission occurs particularly along rivers with dense vegetation along the banks (the so-called gallery forests). Some of the forest species (fusca group) are confined to dense forest and are therefore not normally in contact with livestock, but some also occur on the forest edge and may locally play a significant role as vectors of AAT.
Populations of savannah species feed mainly on mammalian hosts, particularly bovids (antelopes, buffalo, cattle, sheep, goats) and suids (wart hog and bush pig), while riverine tsetse have a very wide range of preferred hosts, including reptiles and humans. Zebras, certain antelopes and also carnivores have little attraction for tsetse flies. The proportion of a tsetse population found infected with pathogenic trypanosomes therefore depends not only on its vector capability, but also on the hosts on which it mainly feeds. For instance, reptiles do not carry pathogenic trypanosomes,15 and there are also major differences between suids and bovids, as the former will infect the flies particularly with T. simiae and T. godfreyi, while bovids are mainly the source of T. vivax and T. congolense).16
Herd management is also important. Daily activity patterns of the tsetse species involved and the grazing patterns of the herds are of great influence. If the herds graze on infested sites at the time of the day that the flies are most active, transmission will occur more frequently. In the Sahel zone, many of the cattle owners (e.g. the Baggara and the Fulani) are transhumant, because in the dry season the pastures and watering places in the Sahel are insufficient to maintain the large livestock populations. The zebu herds, accompanied by small ruminants, are then moved hundreds of kilometres to the south, where they may enter tsetse belts and contract AAT. Although the owners generally know the danger and recognize and associate tsetse flies with the disease, they are not always able to avoid infested areas. Particularly during dry years the southward migration is greater than usual, and the owners may deliberately choose between the risk of starvation of the herd and of tsetse-transmitted trypanosomosis.17 At the beginning of the rainy season the transhumants start to move back to the Sahel pastures, in order to arrive when these are sufficiently lush. The animals infected in the tsetse belts are diseased by the time they reach the rainy season pastures, and may even die before, the physical effort of transhumance adversely affecting the outcome. Unless the animals are treated in time, great losses may occur and when there are large numbers of tabanids and other biting flies around during the rains, the infection may be further transmitted mechanically outside the tsetse belts.
Species and breed susceptibility are of course of great importance. Whereas in tsetse areas trypanosomosis is a very obvious problem in susceptible livestock, it may remain practically inapparent where trypanotolerant breeds are concerned (even if these breeds may not be very productive when challenge is high).
The risk to susceptible ruminants living in comparatively free areas surrounded by tsetse-infested regions, or at the edge of tsetse-belts, varies from year to year. Generally, tsetse fly populations during wet years will increase, spread, and persist during the dry season in areas from where they disappear in dry years.
Also, animals used for transporting persons or goods are sometimes particularly at risk. For example, although the classical breeding areas of camels in Africa are north of the tsetse belts, individual camels are used for the transport of merchandise to transhumant animal owners in their dry season grazing grounds in or near tsetse belts, and these camels risk contracting tsetse-transmitted trypanosomosis. The same applies to the riding horses of travellers and of the transhumant cattle owners. Interestingly, in recent years there has been a tendency in Kenya to start keeping camels as far south as the Masai areas, because of the great losses in cattle caused by the severe droughts in the 1980s; this will of course increase contact between camels and tsetse fly and result in more disease.
The epidemiology of non tsetse-transmitted trypanosomosis (T. evansi, T. vivax18) is also influenced by many factors. There may be seasonal outbreaks, where the populations of biting flies (Tabanids, stable flies, etc.) are influenced by important seasonal climatic differences. The (chronic) disease sometimes becomes more clinically apparent during the dry season, when immunodepressive factors such the poor nutritional state of the animal diminish its defences, even when the initial infection occurred during the rains. The epidemiology is also greatly influenced by host preferences and diurnal (daily) behaviour patterns of the various local species of tabanids and other biting flies (e.g. whether the hours that they are active allow much contact with livestock or not).
The main reservoirs of T. vivax infection in Latin America are probably domestic ruminants themselves, but T. evansi has found new wild reservoirs such as blood-sucking vampire bats and the capybara, a giant rodent. The peculiar involvement of vampire bats in the transmission of T. evansi has been mentioned before in this field guide.
13 The general term epidemiology tends to replace epizootiology, which was in common use in connection with diseases in animals.
14 G. m. morsitans does not occur in Burkina Faso, nor in West Africa as a whole.
15 But tsetse flies do get infected on reptiles with specific reptile trypanosome species, such as T. grayi of crocodiles, a species of the subgenus Megatrypanum (Stercoraria). Such infections may render the microscopical diagnosis of trypanosome infections in tsetse flies difficult (see Chapter 3 - Diagnosis).
16 Host preferences of a tsetse population can be determined in specialized laboratories by serologically identifying the species from which the blood in fed flies originates (blood meal analysis).
17 Ironically, the few herds that remain behind in the Sahel during the dry season and live on the few remaining watering places and the pasture available around these, are usually in better shape at the end of the dry season than the herds returning from the coarse vegetation and the unhealthy areas further south.
18 The epidemiology of dourine, as a venereal disease, is of course very different again, and will not be discussed here.
This section is to some extent a continuation of the previous one on Epidemiology, as many of the factors that determine the distribution of a particular trypanosome species are also involved in epidemiology; in fact, distribution dynamics form an integral part of the epidemiology.
As discussed in the previous section, trypanosomes that are normally cyclically transmitted by tsetse flies, can be transmitted mechanically (see Life cycles), and in the presence of large numbers of biting flies trypanosomosis in domestic animals may extend beyond tsetse belts. Horseflies (tabanids) and stable flies (Stomoxys species) are particularly important as mechanical vectors. Nevertheless, the distribution of nagana in Africa largely coincides with that of its biological vectors, the tsetse flies, and the disease tends to die out in their absence. The presently accepted approximate distribution of the genus Glossina is given in Figure 7; animal trypanosomosis is certainly present in the whole of this area, and in some cases extends to a variable degree beyond it. Within this huge area, the situation is far from uniform. Individual tsetse species (and/or subspecies) are limited to certain regions and have a geographical distribution pattern which is determined by their different climatic and host requirements (just think of the savannah group, the riverine group and the forest group). Trypanosome subspecies, types and even species also have different geographical distribution patterns. For example, T. godfreyi is (so far) only known in the Gambia, T. brucei gambiense occurs in western and Central Africa, T. brucei rhodesiense in eastern and southern Africa, etc.
As far as the individual trypanosome species are concerned, seasonal outbreaks of T. congolense infection have been reported outside tsetse areas in the southern Sudan, for example, associated with large numbers of tabanids, but normally this trypanosome species is confined to tsetse belts and their near surroundings. It has not managed to escape from its biological vector.
The same holds for T. simiae; although it is thought that mechanical transmission by stable flies may be important once the infection has been introduced by tsetse flies into a piggery, the infection is not propagated outside tsetse areas. Knowledge of T. godfreyi is still insufficient.
The case of T. vivax is different. The infection can be seen in Africa at some distance from the edges of tsetse belts, and the author of this book diagnosed the parasite in the late 1950s in sedentary cattle herds all along the White Nile from Malakal in the southern Sudan up into the semi-desert of Khartoum Province, hundreds of kilometres from any tsetse belt. A similar situation has been reported in Ethiopia, where T. vivax is commonly found in highlands too cold for tsetse survival. But the most remarkable fact is that T. vivax has been able to establish itself in the western hemisphere, in the absence of tsetse. These American strains of T. vivax are thoroughly adapted to mechanical transmission and all attempts to transmit them biologically through tsetse have failed. In the past, T. vivax has also been present on the Indian Ocean island of Mauritius, Without tsetse, but has been eradicated there. There are also indications that T. vivax may sometimes persist at a low level, because of mechanical transmission, after tsetse flies have been eradicated from an area.
The distribution of T. brucei seems to be closely associated with that of its Glossina vectors (Figure 7), but it should be remembered that T. evansi, and probably also T. equiperdum, appear to have been derived from T. brucei and have adapted to mechanical and venereal transmission, respectively. T. evansi has been spread widely by biting insects outside tsetse-infested regions in Africa, and also outside Africa; it is present in tropical and subtropical areas of Africa north of the equator, in Asia, and in South and Central America from Panama to Argentina. T. equiperdum infection, as a venereal disease, is even less restricted by climate and in the past has spread as far as Canada and Russia in the northern hemisphere, and as far to the south as Chile and South Africa. Its present distribution is not very well known; T. equiperdum is sometimes difficult to distinguish from T. evansi. It has been eradicated from North America and most of Europe. It is certainly present in northern and southern Africa, and in tropical Africa at least in Ethiopia and probably the Sudan. It has made a comeback (or perhaps has been rediscovered) in Europe (Italy, Russia, possibly other countries), and is still present in parts of Asia, including Ouzbekistan and China. It is also believed to be still present in parts of South America, but there is little reliable information.
Tsetse distribution in Africa