veterinary
parasitology
ELSEVIER
VeterinaryParasitology57 (1995) 19-41
International collaborative research: significance of
tick-borne hemoparasitic diseases to world animal
health
Gerrit Uilenberg
CIRAD-EMV'E, 10 rue Pierre Curie, 94 704 Maisons-Alfort, France
Abstract
A general review is given of the tick-borne hemoparasitic diseases of greatest economic
importance in ruminants, babesiosis, anaplasmosis, theileriosis and cowdriosis, each caused
by one or more species of hemoparasites. Most affected are cattle and small ruminants,
buffalo are more resistant and little is known regarding camels. The situation varies from
one continent or region to another. Innate and breed susceptibility to these diseases are of
tremendous importance. Disease in the field cannot be considered separated from the whole
complex of tick-borne diseases and from the ticks themselves, particularly if the aim is to
attain endemic stability. International coordination is needed now that research funds are
scarce.
An appendix contains tables with hemoparasites of various domestic animals and notes
with background details.
Keywords: Haemoparasites,general
1. Introduction
In this review the term tick-borne hemoparasites includes all tick-borne organisms which are visible with light microscope and which occur in the circulating
blood as part of their normal life-cycle. Tick-borne hemoparasites occur on every
continent and affect all domestic animals. Ticks are the most important ectoparasites of domestic animals, because of the direct damage they can inflict (Uilenberg, 1992). In the veterinary field, protozoan and rickettsial tick-borne diseases
are by far the most important. A few are of zoonotic importance, for instance
Borrelia burgdorferi and Babesia microti, for which a better name would be Theil0304-4017/95/$09.50 © 1995 ElsevierScienceB.V. All rightsreserved
SSDI 0304-4017 ( 94 )03107-X
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G. Uilenberg / Veterinao, Parasitology 57 (1995) 19-41
eria microti, (Mehlhorn and Schein, 1984). Ehrlichia chaffeensis and Ehrlichia
sennetsu are probably also tick-borne zoonoses, although their vectors have not
yet been identified (Ristic and Holland, 1993 ). An important reason for believing them to be zoonoses is that there are no tick species, at least none of the family
of hard ticks, the Ixodidae, which are sufficiently closely associated with the human species for specific human tick-borne diseases to have evolved. As far as soft
ticks, the Argasidae, are concerned, the African tick Ornithodoros moubata, with
its subspecies moubata and porcinus, may be an exception; it lives in close association with humans in huts and transmits human relapsing fever (Borrelia duttoni) for which no animal reservoir appears to be necessary. These ticks may have
adapted to man from their original hosts, the African warthog, with which they
still live in close association, in burrows.
Cowdria ruminantium, causal rickettsia of heartwater in ruminants, can be
grown in human endothelial cells, as reported by Tott6 et al. ( 1993 ). Although
there is no evidence for the ability of C. ruminantium to infect human beings,
and a serological study would even tend to indicate otherwise (Kelly et al., 1992 ),
this observation should stimulate further studies on this point and scientists should
be careful in handling infective material. Moreover, certain strains have a much
wider experimental host range than just ruminants, including rodents (Du Plessis
and Kiimm, 1971; Oberem and Bezuidenhout, 1987). The Senegal isolate used
by Tott6 et al. (1993) is not pathogenic for mice in normal circumstances
(Jongejan et al., 1988).
From a world animal health and especially an economic point of view, tickborne diseases of domestic ruminants (except for camels) are certainly the most
important, but those of pet animals, especially dogs, and of equines, are by no
means negligible. Although anyone dealing with livestock in tropical and subtropical areas of the world needs no telling that tick-borne hemoparasites are important, there are few reliable global figures. It is of little use to repeat here various estimates of losses, which depend on uncertain and variable factors, including
annual climatic variations, fluctuating exchange rates and inflation. The Food
and Agriculture Organization (FAO) estimated in 1984 total annual losses due
to ticks and tick-borne diseases in the world at roughly US$7000 million (7 milliard or 7 billion, depending on the continent you come from), but FAO added
that the total losses may in fact be much higher.
The economically most important hemoparasitic tick-borne diseases of ruminants on a global scale, 'the big four', are certainly bovine babesiosis caused by
Babesia boris and Babesia bigemina, bovine anaplasmosis (Anaplasma marginale), bovine theileriosis caused by Theileria annulata and Theileria parva, and
cowdriosis or heartwater of cattle and small ruminants (Cowdria ruminantium ).
Babesia bigemina is moderately pathogenic for adult cattle, but widely spread in
tropical and subtropical regions of all continents, Babesia boris is highly pathogenic for European breeds, and almost as widely spread, except for large areas in
Africa. Bovine anaplasmosis is even more widely distributed, occurring even in
many temperate areas; its pathogenicity is variable depending on strain virulence; adult dairy cattle commonly die if not treated. Although Theileria parva is
G. Uilenberg / Veterinary Parasitology 57 (1995) 19-41
21
even more virulent than Theileria annulata for exotic stock, the latter is more
important on a global scale as it is much more widely distributed. Theileria parva
is limited to parts of eastern, central and southern Africa, but the distribution of
Theileria annulata encompasses the Mediterranean basin, including large parts
of southern Europe and northern Africa, the Middle East and southern Asia. In
southern Asia it probably does not extend east of the Indian subcontinent, but it
does include parts of southern Siberia and China. It is not clear where the eastern
limit of Theileria annulata (and its Hyalomma vectors) is exactly located, there
has been considerable confusion with Theileria buffeli (see also Table A3). In
northeastern Africa its distribution along the Nile extends at least to the central
Sudan and in West Africa it has recently been shown to occur as far south as
southern Mauritania (Jacquiet et al., 1990). Heartwater (C. ruminantium) is
highly pathogenic for exotic breeds of cattle and small ruminants, but its distribution is limited to (most of ) subsaharan Africa and neighboring islands as well
as three islands in the Caribbean.
In general, the domestic buffalo contracts the same hemoparasites as cattle, but
appears to be less susceptible. Whether the higher resistance is innate in the species as a whole or whether natural selection of populations in endemic areas is an
important factor, has not been examined.
There are other important tick-borne hemoparasitic diseases of ruminants, less
widely distributed, of lesser economic impact or not well identified. Small ruminant theileriosis ( Theileria lestoquardi; the name Theileria hirci, commonly used
for this parasite, is invalid (Morel and Uilenberg, 1981 ) ) and babesiosis, particularly that due to Babesia ovis, are locally of great importance. Anaplasmosis of
small ruminants due to Anaplasma ovis is probably somewhat less so, although it
is more widely spread and individual fatal cases do occur, especially in goats.
Camels do not appear to suffer much from hemoparasitic tick-borne diseases,
although theilerias, babesias and anaplasms have been reported, often not very
convincingly, both in the bactrian and the one-humped camel (Purnell, 1981, see
also Appendix). (However, if one goes beyond the strictly hemoparasitic diseases, tick-induced paralysis may well be important in camels (Musa and Osman,
1990).) Domestic reindeer also suffer from infections with Babesia and/or
Theileria species, of which one has received a specific name (which is either Babesia tarandirangiferis (Kerzelli, 1909) or Theileria tarandirangiferis (Kerzelli,
1909), but it is not clear to which genus it belongs). These parasites have been
briefly reviewed by Uilenberg ( 1981 ).
Two Babesia species have been reported from pigs (Table A2), but they are
not important on a global scale.
Of the domestic Equidae, horses are the most susceptible to tick-borne hemoparasitic diseases of which infections with Babesia caballi and especially Theileria equi (a name which is certainly more correct than Babesia equi, see Table
A4) are the most important on a global scale. They occur on all continents except
for Australia, being transmitted by several species of ticks of the genera Hyalomma, Rhipicephalus and Dermacentor. Recent reports on experimental transmission of Theileria equi by Boophilus microplus (Knowles et al., 1992) may
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explain its presence in Madagascar, where it had to be transmitted either by Amblyomma variegatum, by Boophilus microplus or by Otobius megnini ( Uilenberg,
1967) and in parts of Latin America where there is no other likely vector. This
new experimental vector should also incite Australian scientists to carry out a
thorough survey in their country, where Theileria equi has made a short appearance (Mahoney et al., 1977). Apart from acute disease, chronic infections, especially by Theileria equi, may affect the performance of the animals and relapses
are not uncommon in horses in endemic regions, probably induced by stress factors. Donkeys appear to be much more resistant. Theileria equi also occurs in
wild zebra.
Other tick-borne hemoparasitic diseases are caused by Ehrlichia species (Ehrlichia equi, Ehrlichia risticii) and while these are relatively important in parts of
the USA, on a global scale they do not appear to have a significant impact on
equine health, and I will not go into details here. However, it cannot be excluded
that we are only starting to recognize these diseases elsewhere.
Hemoparasites of pet animals are also of considerable economical importance,
not just because of their traditional role as helpers in hunting, control of vermin,
herding, guarding, etc., but particularly in those (richer) countries where such
animals have an important social and affective role and huge sums are spent on
their upkeep and health. The most widespread diseases of dogs are babesiosis
( Babesia canis and Babesia gibsoni ) and ehrlichiosis ( Ehrlichia canis ). Babesia
canis is not one homogeneous species. Strains transmitted by Rhipicephalus sanguineus occur in most tropical and subtropical regions; they do not protect against
more virulent strains in Europe transmissible by Dermacentor ticks, and both
types do not give protection against even more virulent African strains of which
Haemaphysalis leachii is the vector. At least three subspecies (or perhaps even
species ) may thus be distinguished and names for these have been suggested (see
Table A2). In those areas where Rhipicephalus sanguineus is present, Babesia
canis vogeli and Ehrlichia canis often occur together, and even Babesia gibsoni
may be transmitted by this tick. Another hemoparasite transmitted by the same
tick species is Hepatozoon canis; the real importance and pathogenicity of this
interesting parasite is not quite clear, but it is becoming more and more apparent
that it can be quite a serious pathogen. It is one of the rare examples of a hemoparasite which infects its host by oral ingestion.
Ehrlichia canis is a major health problem for dogs, especially purebred dogs, in
most tropical and subtropical regions of the world, where it is transmitted by the
common brown dog tick, Rhipicephalus sanguineus. Although there are many instances of populations of the dog tick that have settled in buildings in temperate
areas, where they cannot maintain themselves outside, I know of no instance where
such populations are associated with canine ehrlichiosis, at least in Europe.
Symptoms may vary from mild to those of severe tropical pancytopenia. Other
ehrlichial species of dogs (Ehrlichia platys, Ehrlichia ewingii) are mentioned in
the Appendix.
Hemoparasites of cats do not play a great role in feline animal health, at least
G. Uilenberg/ VeterinaryParasitology57 (1995) 19-41
23
not on a global scale. Table A5 reviews the cat piroplasms, but many questions
remain.
Although several tick species act as vectors of various trypanosomes of wild
and even domestic mammals, such as Trypanosoma cervi and other species of the
theileri group, there is no reliable evidence to support claims that they can also
transmit economically important trypanosomes, such as Trypanosorna evansi, and
tick-borne trypanosomes will not be discussed here.
One of the recent 'emerging' tick-borne diseases is Lyme disease. It is of course
not really an emerging disease in the sense that it is increasing and spreading, but
much more a disease the extent of which is only now being discovered. Its zoonotic aspects are considerable, but this borreliosis cannot really be considered as
being a disease of significant importance to world animal health. There are several tick-borne Borrelia spp. in animals and man, most of which are tick-borne.
Amongst the better known ones is Borrelia theileri which infects domestic ruminants and equids in tropical and subtropical regions of the world and is transmitted by ticks such as Boophilus and Rhipicephalus spp. But apart from causing
fever, it is not really pathogenic. As far as I know Borrelia theileri has not yet been
compared with Borrelia burgdorferi. More important from an economical point
of view is avian borreliosis, caused by Borrelia anserina, transmitted by soft ticks
of the Argas persicus complex. It is mainly present in subtropical and tropical
semi-arid regions and can cause considerable economic loss in poultry, especially
if they are housed in hatches and huts which offer good possibilities for the tick
to accomplish its life cycle. Vaccines have been developed in some countries. The
rickettsial agent Aegyptianella pullorum is transmitted by the same ticks and causes
disease, particularly in newly introduced poultry.
Obviously, there is no single answer as to the significance of any tick-borne
disease. The worldwide importance of tick-borne hemoparasites to livestock varies greatly and depends on numerous factors, as has already partly been indicated
above.
2. Factors affecting the importance of tick-borne hemoparasites
2. I. Geographical distribution
Some very virulent diseases, such as East Coast fever in Africa ( Theileria parva
infection of cattle) have a limited distribution, linked to that of its specific vector(s) and may therefore be less important from a global point of view than, for
instance, bovine babesiosis caused by Babesia bigemina, although the case mortality caused by the latter is far lower. However, East Coast fever is locally, in
parts of East Africa, the most important bovine disease, not just the most important tick-borne bovine disease. However, the local significance of tick-borne
hemoparasitic diseases depends not only on the presence or absence of particular
ticks and tick-borne agents, but also on numerous other factors.
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2.2. Type of livestock involved
Because of natural selection pressure, indigenous populations, having lived for
a long time with local ticks and tick-borne diseases, have developed either an
innate resistance or an innate ability to develop a good immune response to the
tick or tick-borne disease in question. Most tick-borne diseases are particularly
important for exotic livestock. For instance, in East Africa, the local shorthorn
zebu lives happily in regions where East Coast fever is endemic, at least in an
endemically stable situation, while case mortality in exotic stock may be 90% or
more. The importance of tropical theileriosis in India has considerably increased
since the start of a massive crossbreeding programme (European cattle X local
zebu), to increase milk production ('Operation Flood'). It should be stressed
that it is not a matter of any fundamental difference between zebu (Bos indicus)
or taurine cattle (Bos taurus). For instance the susceptibility to tropical theileriosis (Theileria annulata) of the local zebu in endemic regions in Asia is low, as
opposed to imported European taurine cattle, while populations of local Bos taurus in the endemic areas of North Africa are also quite resistant to this disease.
Local taurine cattle, such as the N'Dama, in endemic cowdriosis areas of West
Africa have an innate resistance to heartwater, just as the zebu in Madagascar, in
contrast to Asian zebu breeds and European taurines; it all depends on a long
natural selection of the local livestock population by disease pressure. It has been
shown recently that N'Dama cattle, which are trypanotolerant and resistant to
local tick-borne diseases in West Africa, are not resistant to East Coast fever (Dolan et al., 1993).
2.3. Available control methods and their cost
This is also closely linked to the type and the value of livestock involved and
the kind of society we are dealing with. Is the farmer rich enough? Do the susceptibility and the value of the livestock involved justify expensive control methods
(if available)? Is the organization of the veterinary service up to the task? For
instance, in Zambia, Pegram and Chizyuka (1990) have shown that the annual
cost of intensive tick control is greater than the benefit where traditionally managed local Sanga cattle are concerned (apparently in the absence of East Coast
fever).
2.4. Inoculation rate
With most tick-borne diseases there is a period during which young animals
are more resistant than older ones, that is they are as susceptible to infection but
the disease is milder (see below). If the inoculation rate, the infection challenge,
is high enough to infect all young animals during that period, then there is little
or no clinical disease as all potentially vulnerable older animals are already immune; the situation is endemically stable. The inoculation rate depends on the
numbers of ticks present and their infection rate. The inoculation rate may drop
G. Uilenberg / Veterinary Parasitology 57 (1995) 19-41
25
below the level required for an endemically stable situation in areas where the
climate is marginal for the tick vector (and this may vary from year to year depending on fluctuations in rainfall), and in farms or ranches where acaricidal tick
control is intensive. Such a situation may theoretically even arise in a region which
is quite suitable for the vector and where there is no tick control, but where livestock has a very high innate resistance to the tick in question itself; for instance,
zebu cattle may be so resistant to infestation with Boophilus microplus that the
inoculation rate is below the level required for endemic stability for babesiosis
(Mahoney and Ross, 1972 ). (But because of the innate resistance of such cattle
to babesiosis, the fact may not be all that important, especially where Babesia
boris is concerned. ) Resistance to infestation by specific ticks is probably also
not a matter of being zebu or taurine, but of having lived for many generations
with the tick in question, again a matter of natural selection. In Australia the
Asian zebu is far more resistant than European taurines to the Asian tick Boophilus microplus, while in West Africa the local taurine has been reported to carry
lessAmblyomma variegatum ticks than West African zebu (Mattioli et al., 1993 ),
which probably originated from areas further north, too dry for this tick.
2.5. (Inverse) age resistance (see above)
This resistance or tolerance to infection in young animals is independent of
maternal immunity (although in some cases maternal immunity may play an additional role, for instance in Babesia bovis infection (Hall, 1963)). In bovine
babesiosis caused by Babesia boris or Babesia bigemina, as well as in bovine anaplasmosis, this age resistance is generally considered to last some 9 months, and
then to wane gradually. It is much shorter in heartwater, but precise figures are
not available and various authors have put forward periods of 10 days to 6 weeks,
depending on the animal species; the numbers of animals on which these figures
are based are small.
2.6. Strain virulence
There may be pronounced differences in virulence between isolates or strains
of a tick-borne hemoparasite, but strains of low and high virulence usually occur
in one and the same region. Babesia bigemina may be an exception; it is considered of little importance in Australia, but fatal cases are not uncommon in East
Africa for instance. However, it might also partly be a matter of comparison with
the more pathogenic Babesia boris (at least more pathogenic for European cattle), which is dominant in Australia but absent from much of Africa, as the most
common Boophilus species in Africa is not a vector ofBabesia bovis, only of Babesia bigemina (Potgieter, 1977, cited in De Vos, 1979 and Norval et al., 1983 ).
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3. Loss of potential production
The economic importance of a tick-borne disease is not always limited to the
actual losses caused directly by loss of production and mortality, or indirectly
through the cost of control. Another important point which is not always taken
into consideration is the loss of potential production: In many regions local livestock has adapted itself to local hemoparasites. However, the productivity of such
livestock is often low, and in many cases these hemoparasites defeat attempts at
improving productivity by introducing far more susceptible exotic stock on a significant scale. The problems can of course be overcome by intensive tick control
and good veterinary care, using immunization and treatment; however, good (or
even poor) veterinary care is far from universally available, while acaricide resistance is increasingly a problem in tick control. And where the infrastructure does
make this approach possible, the cost of prevention takes away part of the gain
associated with increased productivity. In much of subsaharan Africa where diseases such as East Coast fever and heartwater are rife, the loss of potential production is enormous, and the same applies to the extensive regions where Theileria annulata is a dominant factor. In the western hemisphere, Guadeloupe is an
outstanding example of loss of potential production because of the presence of
the African tick Amblyomma variegatum, and the problems associated with it,
heartwater and severe dermatophilosis (although Dermatophilus congolensis is
not a hemoparasite and is not even transmitted by Amblyomma variegatum, the
presence of this tick somehow allows the development of severe forms of dermatophilosis in susceptible livestock) (Uilenberg, 1992). The present annual loss
(including the cost of tick control) due to the presence of the tick on the island
has been estimated at some US$1.5 million (Camus and Barrr, 1990), but the
loss of potential production is far higher: of the 75 000 cattle on the island over
90% are very resistant Creole cattle, while only 1% is made up of far more productive pure exotic breeds. This composition of the cattle population is, in the
Caribbean, peculiar for Guadeloupe because of the selective pressure maintained
by the tick, cowdriosis and dermatophilosis since the tick was introduced.
4. Future research
Many scientists work on one particular hemoparasitic disease and usually even
on only one particular aspect of a disease. This is of course to a large extent unavoidable because of the rapidly accumulating amount of knowledge and the development of new, sophisticated techniques, which necessarily lead to increasing
specialization. Nevertheless, it should be realized that the control of any particular tick-borne hemoparasitic disease can never be considered in isolation from
its tick vector(s) and, depending on the region, from other tick-borne and tickassociated diseases and their vectors. An effective method of immunization against
one important tick-borne disease such as East Coast fever will not necessarily in
itself have much impact on production if susceptible exotic cattle continue to be
G. Uilenberg / Veterinary Parasitology 57 (1995) 19-41
27
exposed to other tick-borne diseases, such as heartwater, and to debilitating numbers of ticks (Uilenberg, 1985 ). If on those Caribbean islands where heartwater
exists one were to adopt immunization against this disease as the only means of
control, without controlling the tick vector, the problem of the disease might to a
great extent be solved, but severe dermatophilosis would still cause havoc among
susceptible cattle. On the other hand, were one to control heartwater by intensive
tick control, then endemic stability to bovine babesiosis and anaplasmosis, transmitted in the Caribbean by Boophilus microplus, would be disrupted and adult
cattle would be vulnerable (George, 1991 ); immunization against these diseases
could then be necessary, especially as acaricide resistance in Boophilus ticks is
particularly common. On the other hand, if one intends to achieve endemic stability to tick-borne diseases, which implies at most limited tick control, diseases
such as East Coast fever might spread again to areas where it has been eradicated
but where the vector still occurs (in large parts of southern Africa). Norval et al.
( 1992 ) describe and discuss in an interesting paper the advantages and dangers
associated with a change from compulsory short-interval dipping to reduced dipping and a return to endemic stability; they consider the possible spread of heartwater with its vector as the greatest danger, but a return of classical East Coast
fever, which still occurs for instance in neighboring Zambia for example, could
be even more important. In areas where severe dermatophilosis is associated with
Amblyomma ticks, a reduction of the intensity of dipping might make it possible
to achieve endemic stability for several of the tick-borne diseases, but severe dermatophilosis would increase. These are but a few examples of the complexity of
the problem in many parts of the word.
Which additional knowledge is most urgently required to improve the control
of hemoparasitic tick-borne diseases? With the ever increasing cost of acaricidal
tick control, associated with the great problems of acaricide resistance, it appears
logical to pay more attention to alternative methods of control. These include
making use of the immunological response to tick-borne diseases and to ticks
themselves.
4.1. Vaccines against tick-borne diseases
Infection and treatment methods of immunization exist against many of the
tick-borne diseases of cattle, such as babesiosis due to Babesia boris and Babesia
bigemina, East Coast fever, tropical theileriosis and heartwater. Live naturally
mild or artificially attenuated parasites are used against tropical theileriosis
(schizont-infected lymphoblast cultures) and anaplasmosis, as well as against
Babesia boris and Babesia bigemina, while an attenuated in vitro grown heartwater vaccine is under experimentation (Jongejan et al., 1993 ). These methods have
obvious inconveniences, risks and imperfections. Live material is vulnerable and
needs a continuous cold chain (although in the case of the rickettsial diseases the
possibility of lyophilizing the material may help (du Plessis et al., 1990). The
virulence of the inoculum used for infection and treatment methods and possible
reversion to virulence of attenuated material always remain a danger. Infected
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blood is normally used, except for in vitro grown material, and entails great risks
of spreading other bloodborne infections. Several examples of such spread exist.
For all these reasons inactivated, molecular or recombinant vaccines would
present undeniable advantages, but could also have certain disadvantages. Inactivated and molecular vaccines often induce a shorter immunity than that caused
by live material; the problems of antigenic diversity, which are for instance very
important in East Coast fever and heartwater, could well become more pronounced than with the use of live organisms. Even for anaplasmosis and babesiosis, where antigenic diversity is not a major problem when live vaccines are
used, strain differences might cause the results of new vaccines to be unsatisfactory. Even the use of a live Babesia boris vaccine in Australia is thought to have
resulted in the selection of antigenically different strains (Bock et al., 1992 ). Killed
Anaplasma vaccines may also give less protection against heterologous strains
(Kuttler et al., 1984 ).
Then there is the problem of cost, which may not be all important in more
developed systems of animal production and for pet animals, but could be a disadvantage in less developed countries, where veterinary services are accustomed
to using infection and treatment methods, for which no patents exist. Whether
the final cost is really lower remains to be seen, as the cost of maintaining live
strains and the salaries of the government employees involved are not usually
taken into account.
There are as yet very few examples of inactivated vaccines which are available
for routine use against tick-borne hemoparasitic diseases, and no molecular or
recombinant ones, as far as I know, although several teams carry out intensive
research on such vaccines against important diseases such as bovine babesiosis
( Babesia boris), theileriosis (Theileria parva and Theileria annulata ) , anaplasmosis and heartwater.
There is a commercial vaccine against canine babesiosis based on soluble antigens of cultured material of European Babesia c. canis; there are mixed opinions
on its efficacy and it is very unlikely to be of any use against African Babesia canis
rossi. An inactivated vaccine against bovine anaplasmosis has been on the American market for many years, but apart from the fact that it was not practical for
use in extensive livestock keeping, because it had to be administered repeatedly,
the erythrocytic material it contained was responsible for cases of neonatal isohemolytic anemia.
4.2. Vaccines against tick infestation
The Australian molecular vaccine against the tick Boophilus microplus has been
provisionally released on the Australian market and appears to hold great promise (Willadsen, 1990 ). Confirmation of its success and economic viability would
considerably raise the hope of attaining similar vaccines for other tick genera and
species. At present the situation is far less advanced where other ticks are
concerned.
G. Uilenberg / Veterinary Parasitology 57 (1995) 19-41
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4.3. Make use of innate resistance to tick-borne diseases and to tick infestation
As mentioned earlier, there are considerable differences between livestock populations and individual animals in their capability of tolerating infection with
various tick-borne disease agents and also to limit tick infestation itself. Unfortunately these resistant indigenous populations are usually not very productive.
Selection on higher productivity within such populations is of course possible,
but likely to take a very long time, especially because maintaining or improving
the innate resistance is a priority.
Cross-breeding with more productive breeds is a short-cut, but still needs to be
followed by lengthy selection for both resistance and productivity. Selection should
of course be preceded by a thorough study of the heritability of the resistance
trait. Selection could be faster if genetic markers for resistance can be found, but
the search for such markers is only likely to be successful if single or only few
genes are involved. This may well be different from one disease to the other.
Finally, and again only if single or few genes are involved, one might dream
about the possibility of transfer of resistance genes.
5. Conclusion
It is difficult to interest the private industry in diseases which do not directly
concern the richer countries, as the potential market is often small and certainly
poor. Public research funds have become more difficult to obtain in the present
economic context. This means that priorities have to be set and international
coordination is indicated, in order to use the available funds as efficiently as possible. The coordinating role of international organizations such as FAO, OIE and
the CGIAR system, is more important than ever, and these organizations should
increasingly define and coordinate their tasks amongst themselves. This is certainly easier said than done.
References
Aiani, A.J. and Herbert, I.V., 1988. Morphology and transmission of Theileria recondita (Theileriidae: Sporozoa) isolated from Haernaphysalis punctata from North Wales. Vet. Parasitol., 28: 283291.
Anderson, B.E., Dawson, J.E., Jones, D.C. and Wilson, K.H., 1991. Ehrlichia chaffeensis, a new species associated with human ehrlichiosis. J. Clin. Microbiol., 29: 2838-2842.
Anderson, B.E., Greene, C.E., Jones, D.C. and Dawson, J.E., 1992. Ehrlichia ewingii sp. nov., the
etiologic agent of canine granulocytic ehrlichiosis. Int. J. Syst. Bacteriol., 42: 299-302.
Bock, R.E., de Vos, A.J., Kingston, T.G., Shiels, I.A. and Dalgliesh, R.J., 1992. Investigations of
breakdowns in protection provided by living Babesia boris vaccine. Vet. Parasitol., 43: 45-56.
Boussarie, D., 1982. Un cas de piroplasmose avec des parasites d'un aspect particulier. Anim. Compagnie, 17: 597.-599.
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Appendix: Tick-borne hemoparasites of domestic animals
Table AI
Babesia species of domestic ruminants ~
Species
Domestic hosts
Vectors
Disease
Known
distribution
B. beliceriAbramov
& Djakonov, 1974
B. bigemina (Smith
& Kilborne, 1893 )
Cattle
Hyalomma
9
Russia
Cattle, buffalo
Boophilusspp.,
Rhipicephalus bursa
Redwater,
babesiosis
B. bovis Starcovici,
1893
Cattle, buffalo
Boophilusspp.,
Rhipicephalus bursa
Redwater,
babesiosis
B. crassa HashemiFesharki &
Uilenberg, 198 l
B. divergens
(M'Fadyean &
Stockman, 1911 )
B. jakimovi
Nikolskii et al.,
19774
B. major ( Sergent et
al., 1926 )
B. motasi Wenyon,
1926
B. occultansGray &
de Vos, 19816
B. ovata Minami &
Ishihara, 19807
B. ovis Starcovici,
18938
Sheep, goats
Unknown
Probably mild
Africa,
America, Asia,
Australia,
Europe 2
Africa,
America, Asia,
Australia,
Europe ~
lran
Cattle
lxodes ricinus
Redwater,
babesiosis
Europe
Cattle, reindeer
Ixodes spp.?
Babesiosis
Siberia
Cattle
Cattle
Hyalomma spp.
Bovine
babesiosis
Sheep and goat
babesiosis
Mild
Europe
Sheep, goats
Haemaphysalis
punctata
Haemaphysalisspp.
Cattle
Haemaphysalis
longicornis
Rhipicephalusbursa
Sheep, goats
Bovine
babesiosis
Sheep and goat
babesiosis
Africa, Asia,
Europe 5
Africa
Eastern Asia
Africa, Asia,
Europe
G. Uilenberg / Veterinary Parasitology 57 (1995) 19-41
31
Table A2
Babesia species of other domestic animals (for cats, see Table AS)
Species
Domestic hosts
Known vectors
Disease
Known
distribution
B. caballi
(Nuttall &
Strickland,
1910)
B. canis (Piana
& GalliValerio, 1895 )
Horse, donkey,
mule
Hyalomma,
Rhipicephalus,
Dermacentor spp.
Equine
babesiosis
Africa,
America, Asia,
Europe
Dog
Dermacentor,
Rhipicephalus,
Canine
babesiosis
B. gibsoni
(Patton, 1910)
Dog
B. perroncitoi
(Cerruti, 1939)
B. trautmanni
(Knuth & Du
Toit, 1921 )
Pig
Haemaphysalis,
Rhipicephalus
sanguineus Io
?
Pig
Rhipicephalus spp.
Africa,
America, Asia,
Australia,
Europe 9
Africa,
America, Asia,
Europe 11
Europe (Italy),
Africa 12
Africa, Europe
Haemaphysaliss p p . 9
Canine
babesiosis
Porcine
babesiosis
Porcine
babesiosis
Table A3
Theileria species of cattle
Species
Domestic hosts
Known vectors
Disease
Distribution
T. annulata
(Dschunkowsky
& Luhs, 1904)
T. buffeli
NeveuLemaire,
191213
T. mutans
(Theiler, 1906 )
Cattle, Asian
buffalo
Hyalomma spp.
Africa, Asia,
Europe
Cattle, domestic
buffalo
Haemaphysalis
spp. ~4
Cattle (original
host Cape
buffalo )
Cattle, domestic
buffalo
(original host
Cape buffalo)
Cattle (original
host eland
antelope )
Amblyomma spp.
Cattle (original
host Cape
buffalo )
Amblyornma spp.
Mediterranean
or tropical
theileriosis
Oriental or
cosmopolitan
benign
theileriosisis
Benign African
bont tick
theileriosis
East Coast
fever, Corridor
disease, January
disease18
Benign African
rhipicephaline
theileriosis,
Tzaneen disease
Nonpathogenic
T. parva
(Theiler,
1904) 1~
T. taurotragi
(Martin &
Brocklesby,
1960)
T. velifera
(Uilenberg,
1964 )
Rhipicephalus spp.
Rhipicephalus spp.
Africa,
America~6,
Asia, Australia,
Europe
Africa,
Caribbean
Africa
Africa
Africa,
Caribbean
32
G. Uilenberg / Veterinary Parasitology 5 7 (1995) 19-41
Table A4
Theileria species of other domestic animals
Species
Domestic hosts
Known vectors
Disease
Known
distribution
T. camelensis
Bactrian camel
?
?
Asia
Yakimoff, 1917
T. dromedarii
One-humped
camel
?
?
Asia
Mishra et al.,
198719
T. equi (Laveran,
1901 )20
Horse, donkey,
mule
Equine
'babesiosis'
'nuttalliosis'
Africa,
America,
Asia, Europe
T. lestoquardi
Sheep, goat
Hyalomma,
Rhipicephalus,
Dermacentor
spp., Boophilus
microplus
ttyalomma spp.
Small ruminant
theileriosis
Africa, Asia,
Europe
Sheep, goat
~2J
No disease
T. separata
Sheep (goat)
No disease
(Uilenberg and
Andreasen, 1974 )
Theileria sp. 22
Rhipicephalus
evertsi
Africa, Asia,
Europe 21
Africa
Sheep (goat)
Haemaphysalis
punctata
No disease
Europe
Morel &
Uilenberg, 1981
T. ovis Rodhain,
19162 J
Table A5
Piroplasmids of cats
Species
Hosts a
Type 23
Disease
Known
distribution
B. cati
Wild cat (not
infective for
domestic cat 24)
Wild cat,
domestic cat,
leopard, lion,
cheetah 25
Jaguarundi
(domestic cat,
dog, fox)
Leopard
(domestic cat) 26
Paired
?
India
Theileria-type
Feline
babesiosis
Africa, ? Asia2%
? Europe
Large, paired
~
South America
(Venezuela)
large, paired
~
Africa (Kenya)
Schizonts in
macrophages,
maltese crosses
in red cells
Fatal for
domestic cat
North America
Mudaliar et al.,
1950
B. felis Davies,
1929
B. herpailuri
Dennig, 1967
B. pantherae
Dennig &
Brocklesby,
1972
Cytauxzoon
felis Kier et
al., 198227
Domestic cat,
bobcat (original
host )
(Maltese
crosses)
aSpecies in parentheses are experimental hosts.
G. Uilenberg / Veterinary Parasitology 5 7 (1995) 19-41
33
Table A6
A naplasma species of domestic animals
Species
Domestic hosts
Known vectors
Disease
Distribution
A. centrale
Theiler, 1911
Cattle
Rhipicephalus
simus
Mild bovine
anaplasmosis
A. marginale
Theiler, 191029
Cattle, domestic
buffalo (sheep,
goats, antelopes,
Cape buffalo,
and other
Bovidae,
Cervidae )
Bovine
anaplasmosis
A. mesaeterum
Uilenberg et al.,
1979
Sheep, goats
(deer)
Boophilus,
Dermacentor,
Hyalomma,
Ixodes,
Rhipicephalus
spp., mechanical
transmission by
biting insects etc.
Unknown
South Africa,
most other
tropical and
subtropical
regions28
All continents,
including several
temperature
regions
A, ovis Di
Sheep, goats
Domizio, 19193~ (antelopes)
?Rhipicephalus
bursa?
?Ornithodoros
lahorensis? 32
Pathogenicity for
sheep not well
studied, nonpathogenic for
goats3°
Small ruminant
anaplasmosis
Europe (the
Netherlands,
Germany)
Africa, Asia,
America, Europe
34
G. Uilenberg / Veterinary Parasitology 57 (1995) 19-41
Table A7
Ehrlichia species of domestic animals: E., "subgenus' Ehrlichia; C., 'subgenus' Cytoecetes 33
Species
Domestic hosts a
Known vectors
Disease
Known
distribution
E. (E.) boris
Cattle, domestic
buffalo, ?pig?34
( sheep, monkey )
Amb/yomma,
Hyalomma,
Rhipicephalus
Mostly mild 35
Africa,
America
(Brazil), Asia
Canine
ehrlichiosis,
tropical canine
pancytopenia
Equine
granulocytic
ehrlichiosis
Canine
ehrlichiosis
(milder than
that caused by
Africa,
America, Asia,
Europe
(Donatien &
Lestoquard,
1936)
E. (E.) canis
spp.
Dog
Rhipicephalus
sanguineus
Horse, donkey
(sheep, goat,
dog, monkey )
Dog
Unknown
(Donatien &
Lestoquard,
1935 )
E. (C.) equi
Lewis et al.,
197536
E. (C.) ewingii
Anderson et al.,
1992
Amblyomma
americanum
America
Europe 37
America
E. canis )
E. (C.) ondiri
Cattle (sheep) 38
Unknown
Sheep, goat
Rhipicephalus
(Krauss et al.,
1972)
E. (E.) ovina
(Lestoquard &
Donatien, 1936 )
E. (C.)
phagocytophila
Ondiri disease
( =bovine
petechial fever)
Mostly mild 39
Africa (Kenya)
Africa, Asia
spp.
Cattle, sheep,
goats 4°
Ixodes ricinus
Tick-borne
fever
Europe
Dogs
Unknwon
America,
Europe
Horses
Unknown 42
Thrombocytopenia, infection
mostly mild 41
Potomac horse
fever
(Foggie, 1951 )
E. platys French
& Harvey, 198335
E. (E.) risticii
Holland et al.,
1985
America,
Europe,
?Australia? 42
aSpecies in parentheses are experimental hosts.
~Comparative studies using modern methodology and tools are needed to determine the relationship
between Babesia beliceri, Babesia jakimovi, Babesia occultans and Babesia ovata amongst themselves
and with the 'classical' four species of cattle Babesia bigemina, Babesia bovis, Babesia divergens and
Babesia major and also with species of wild herbivores, such as Babesia capreoli Enigk and Friedhoff,
1962, Babesia odocoilei Emerson and Wright, 1968 and the species recently described in desert bighorn sheep (Goffet al., 1993). It is not clear whether Piroplasma taylori Sarwar, 1935, described in
India in a goat, refers to a Babesia or a Theileria. The description is based on smears taken after death
and the pictures clearly show postmortem changes (Sarwar, 1935 ).
~Tropical and subtropical regions.
3Boophilus decoloratus is not a vector, and Babesia boris is therefore absent from those large parts of
Africa, where this tick is the only species of the genus.
4particulars of this species, of which the original hosts might be deer, is based on Purnell ( 1981 ),
whose description of the parasite stems directly from the Russian paper by Nikol'skii et al. (1977).
G. Uilenberg / Veterinary Parasitology 57 (1995) 19-41
35
Table A7 (continued)
5There are considerable differences between parasites grouped under the name Babesia motasi, as
regards serodemes and pathogenicity and there may be more than one species grouped under this
name (Lewis et al., 1981 ). Parasites designated by this name in Africa south of the Sahara are unlikely
to be transmitted by Haemaphysalis spp., and appear to have a morphology intermediate between
classical Babesia motasi and Babesia ovis. Babesiafoliata Ray and Raghavachari, 1941, described in
India, could be a synonym of Babesia motasi.
6Babesia occultans has unfortunately not been compared with Babesia beliceri and there is no strict
proof that it is a new species. The descriptions of their morphology are similar and both have Hyalomma ticks as vectors.
7Babesia ovata is distinguished from Babesia major mainly by serological tests, but is very similar in
morphology and their respective vectors belong to the same vector genus. A similar parasite transmitted by Haemaphysalis longicornis in China is considered to be Babesia major (Lu et al., 1990 ).
SA Babesia ovis.like parasite has been found in sheep in Scotland by Reid et al., 1976, but its identity
is not clear.
9Differences between parasites grouped as Babesia canis are so great that separate species or subspecies can be distinguished, Babesia canis canis transmitted by Dermacentor ticks, Babesia canis vogeli
with Rhipicephalus as vectors, and Babesia canis rossi transmitted by Haemaphysalis (Uilenberg et
al., 1989). Babesia canis canis is limited to Europe and possibly parts of Asia, Babesia canis rossi
occurs in Africa, while Babesia canis vogeli occurs in Africa, America, Asia, Australia and Europe.
1°In the case ofR. sanguineus only transstadial transmission has been reported (Sen, 1933 ).
~'Babesia gibsoni is particularly common in southern and eastern Asia, but it also occurs in Africa,
but appears to be extending its distribution in North America (Conrad et al., 1991 ) and there are
isolated reports of autochthonous infections in dogs by small Babesiae in France (Boussarie, 1982;
Krooshofet al., 1984).
12It is becoming apparent that this parasite is more widely spread, at least in Africa, than was previously known (Purnell, 1981 ). An important epidemic in pigs has been reported in Senegal (Vercruysse and Parent, 1981 ).
13The name Theileria buffeli may be valid for this parasite, with Theileria orientalis as a synonym.
However, it has been suggested that more than one species might be grouped under the same name
(Kawazu et al., 1992a,b,c; Uilenberg et al., 1993 ). The name Theileria sergenti is undoubtedly invalid
(Morel and Uilenberg, 1981 ).
14The vectors in America and Africa are unknown, but highly unlikely to be Haemaphysalis spp. A
recent paper (Fujisaki et al., 1993) reports experimental transmission of Japanese 'Theileria sergentl~
( = Theileria buffeli) by sucking lice, possibly by regurgitation of infected blood. The authors suggest
further studies on a possible role of sucking lice in the epidemiology of this infection.
~SInfection in cattle is usually mild or even symptomless, except in eastern Asia where more pathogenic strains occur. The situation regarding African strains is not yet clear. No disease has been reported in domestic buffalo.
~6In the western hemisphere, so far Theileria buffeli or Theileria buffeli-like parasites are only known
to occur in North America. Theileria mutans and Theileria velifera are present in the Lesser Antilles
(Guadeloupe and Martinique), the status of theilerial parasites reported from other parts of the western hemisphere is not yet clear.
~TThe name Theileria kochi (Stephens and Christophers, 1903) has in fact priority over Theileria
parva (Theiler, 1904).
18Three subspecies or biological types are distinguished in Theileria parva, Theileria parva lawrencei,
causing Corridor or buffalo disease in cattle, Theileria parva parva, the agent of classical East Coast
fever, and Theileria parva bovis, cause of January disease.
19Mishra et al. ( 1987 ) considered the name Theileria camelensis as questionable and described Theileria dromedarii. We concur that the validity of the former is uncertain (cf. Uilenberg, 1981 ), but are
not convinced of the validity of Theileria dromedarii: a surprisingly high percentage of the camels
selected at random were positive not only for intraerythrocytic piroplasms but also for macro- and
microschizonts, which in other ruminants are only readily found in acute cases; the microphotographs
are also unconvincing.
2°The life cycle of this parasite and several other characters are those of a Theileria, not of a Babesia
(Mehlhorn and Schein, 1984 ).
36
G. Uilenberg / Veterinary Parasitology 5 7 (1995) 19-4 I
Table A7 (continued)
2~Theileria ovis and Theileria ovis-like parasites have been reported to be transmitted by several genera and species of ticks, but there is considerable confusion in the taxonomy of nonpathogenic theilerias of small ruminants (cf. Uilenberg, 1981 ). Theileria ovis was originally described in tropical
Africa. The Theileria ovis-like parasite in the Mediterranean basin has Rhipicephalus bursa as a vector.
22Alani and Herbert (1988) have not made it clear why they used the name Theileria recondita for
this parasite, unless they simply followed the lead of Enigk, who reported the same parasite under that
name in 1953 in Germany. The species studied by these authors is certainly different from the parasite
described as Theileria recondita by Lestoquard, 1929 in the Mediterranean basin (cf. Uilenberg, 1981 ).
23The descriptions are not always sufficiently clear. Small Theileria (Maltese crosses) type of parasites, formerly called Nuttallia, are unlikely to be Babesia, and may be either Theileria or Cytauxzoon.
24Levine ( 1985 ) stated that this species occurs in wild and domestic cats, but the single transmission
experiment from wild to a domestic cat by Mudaliar et al. (1950) was unsuccessful.
~SThere is no experimental proof of the identity of these parasites in the domestic cat with those in
the wild Felidae. Babesiafelis could be transmitted from Davies' wild cat to the domestic cat, as could
similar parasites found in lion and leopard, but no attempts appear to have been made to transmit the
morphologically similar parasite which causes feline babesiosis in the domestic cat in southern Africa
to wild Felidae. Similar parasites have also been seen in a bobcat in a zoo. Small piroplasms have also
been described, in insufficient detail, in pumas in a zoo, in a leopard in India, in the serval cat in
Tanzania and in a domestic cat in France.
26Similar large paired typical Babesia have also been seen in lions in South Africa and a domestic cat
in Zimbabwe.
27The name Cytauxzoonfelis was first given in a Ph.D. thesis (Kier-Schroeder, 1979), but this document does not answer the requirements of the International Code for Zoological Nomenclature.
2SAnaplasrna centrale was originally discovered in South Africa (Theiler, 1911 ). It has been spread in
Africa, Australia, southern and eastern Asia and in many countries of Latin America by its use as a
live vaccine against anaplasmosis caused by Anaplasma marginale. It is likely that strains with the
same morphology (i.e. anaplasms situated predominantly not on the edge of the red cell), already
occurred in eastern Asia, but if so, it is not clear whether such local strains are also less virulent than
typical Anaplasma marginale. It is to be noted that there are strains with intermediate morphology
(approximately half of the organisms touching the edge of the red cell, instead of some 70% in typical
A naplasma marginale and some 30% in A naplasma centrale, but such strains are not particularly mild
(unpublished observations on a Texas strain received from Dr. K.L. Kuttler).
29Paranaplasma Kreier and Ristic, 1963, is now generally considered to be a synonym of Anaplasma,
and Paranaplasma caudatum Kreier and Ristic, 1963 (and Paranaplasma discoides) to be a synonym
of Anaplasma marginale, Paranaplasma caudatum was created because certain staining methods
showed the existence of an intraerythrocytic appendage to the anaplasm, and because of antigenic
differences with a strain of Anaplasma marginale. Manifestation of the appendage has since been
shown to depend on the host species (present in bovine, but not in deer erythrocytes) (Carson et al.,
1974 ), and is not part of the organism but rather results from organization of proteinaceous materials
in parasitized bovine erythrocytes (Simpson et al., 1965 ) (cf. crystalloid inclusions in red cells parasitized by certain Theileria species (Van Vorstenbosch et al., 1978; Young et al., 1978; Simpson et
al., 1980) and Haemobartonella fells (Simpson et al., 1978). A separate genus name therefore is
unjustified. Furthermore, immunological differences between strains of Anaplasma marginale are
known to occur, and do not justify in themselves the creation of separate species.
3°Pathogenic for splenectomized sheep, significant anemia was caused in an intact sheep (Uilenberg
et al., 1979).
3tAnaplasma ovis was later redescribed under the same name by Lestoquard (1924). A naplasma ovis
Di Domizio, 1919, has priority.
32Records of transovarial transmission of Anaplasma ovis by ticks should be considered as doubtful,
as Anaplasma marginale and Anaplasma centrale are only transmitted transstadially. Not even the
reports on transstadial transmission by R. bursa and Ornithodoros lahorensis by Rastegaieff (1933
and 1935, respectively ), are really convincing, as the incubation periods were incredibly short, 3 days
and 5 days respectively!
G. Uilenberg / Veterinary Parasitology 5 7 (1995) 19-41
37
Table A7 (continued)
33Some authors distinguish between the genera Ehrlichia (parasites of mononuclear cells) and Cytoecetes (infecting granulocytes). However, there is no strict dividing line between both groups and for
instance a small proportion of E. canis organisms, a parasite of mononuclear cells, is found in granulocytes. Ehrlichia platys, a parasite of thrombocytes of dogs, cannot be assigned on this basis to one of
the genera. The use of these names on a genus or even a subgenus level is debatable also in view of the
fact that on the basis of a comparison of 16S rRNA sequences Ehrlichia (Ehrlichia) canis and E. (E.)
chaffeensis are much more closely related to Ehrlichia (Cytoecetes) ewingii than are E. (C.) phagocytophila and E. (C.) equi (Anderson et al., 1992). In order to indicate the main host cells of a
particular parasite, we use these two names as subgenera in this table, but they should not be taken as
having any official taxonomic status.
a4Tbe observations of Rioche and Bourdin (1968) in Senegal point to the possibility that E. bovis
may cause disease in (European) pigs, but the identity of the Ehrlichia causing this disease in pigs as
E. bovis is still needed. A pathogenic Ehrlichia sp. of pigs has been described in Algeria as Ehrlichia
suis (Donatien and Gayot, 1943 ), which occurred in monocytes and endothelial cells.
35Bovine mononuclear ehrlichiosis is mainly a mild disease, but in certain regions exotic cattle may
suffer from clinical and even fatal disease. More than one species of Ehrlichia might be involved
(reviewed by Uilenberg, 1993 ).
36According to Anderson et al. ( 1991 ) E. equi and E. phagocytophila should be considered as one
species, on the basis of a comparison of the 16S ribosomal sequences, but this does not take into
account that there are definite host differences, as E. equi (in North America) is not infective for
cattle. The infectivity for ruminants of ehrlichial parasites in granulocytes of horses in Europe has not
yet been investigated.
37There is no proof that the Ehrlichia found in granulocytes in horses in Europe is identical with
American E. equi. The infectivity of European E. phagocytophila for horses has not been studied, as
far as I know.
3SEhrlichia ondiri has also been isolated from bushbuck, and is likely to be a parasite of African antelopes which may cause disease in European cattle, although disease in Masai cattle in southern Kenya
has also been associated with the presence ofEhrlichia sp. in granulocytes in Kenya (G. Moll and A.
Lohding, unpublished data, 1987 ). Bovine petechial fever has recently been reviewed by Scott and
Woldehiwet (1993).
39Ehrlichia ovina is accused of causing fatal disease in sahelian sheep in Senegal, introduced into a
more humid area (Gueye et al., 1989).
4°Ehrlichia phagocytophila also occur in species of deer. Tickborne fever has recently been reviewed
by Woldehiwet and Scott, 1993.
41Ehrlichia platys has recently been reviewed by French and Harvey ( 1993 ). Clinical disease may be
caused by certain strains.
42The tickborne nature of Potomac horse fever is not certain. The report on its occurrence in Australia
is solely based on serological evidence. The disease has recently been reviewed by Holland and Ristic
(1993).
38
G. Uilenberg / Veterinary Parasitology 57 (1995) 19-41
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