Three Hyalomma
ticks, namely Hyalomma marginatum rufipes,
Hyalomma marginatum turanicum and Hyalomma truncatum occur in South
Africa. In the 20 years since 1981, when the first case of Crimean Congo
haemorrhagic fever (CCHF) was recognised in this country, human infections have
been more frequently associated with these ticks than with any other cause.
Since 1981 all confirmed human cases of CCHF have been recorded and the actual
or potential sources of infection and the localities at which infection
occurred noted. Ticks have been collected from a variety of domestic and wild
animals across the country and the intensity of infestation with Hyalomma spp. on these animals
determined. Large mammals are the preferred hosts of adult ticks and scrub
hares of the immature stages. The mean burdens of H. marginatum rufipes on all host species and the proportion of
animals infested are greater in the central semi-arid regions of the country
than in the moister east or more arid western regions. The distribution of
human cases of CCHF follows that of the higher intensities of infestation with
this tick species. The concurrence of the highest intensities of infestation
with ticks, a high prevalence of antibodies in preferred host animals, and the
greatest number of CCHF cases in humans in the central, semi-arid regions,
support the contention that H. marginatum
rufipes is the major vector of the virus in South Africa.
The first case of Crimean-Congo haemorrhagic
fever (CCHF) to be recognised in South Africa was diagnosed in a child who had
attended a nature study course (veld-school) in a nature reserve in the North
West Province during February 1981. Surveys to detect virus in ticks and
animals and antibodies in animals and humans in the reserve and its vicinity
were conducted soon thereafter (Swanepoel et al., 1983), and the
seasonal activity of ixodid ticks and their host preferences in the reserve
were determined by and Rechav et al., (1987). Despite the disease being
diagnosed in South Africa for the first time only in 1981, there is little
doubt that it was present in the country long before then as antibodies were
found in sera that had been in cold storage since 1964 (Swanepoel 1994).
The distributions of the three Hyalomma ticks occurring in South
Africa, namely Hyalomma marginatum
rufipes, Hyalomma marginatum
turanicum and Hyalomma truncatum
have been plotted by Theiler (1956) and illustrated by Howell et al.,
(1978), and their hosts listed by Theiler (1962) and Walker (1991). These ticks
are widespread in South Africa and the greatest concentrations occur in
semi-arid in-land regions extending to the western coast with few if any ticks
present in the eastern and southern coastal areas. The preferred hosts of the
adult ticks are large animals such as zebras, eland, domestic cattle, African
buffaloes, rhinoceroses, giraffes and ostriches (Norval 1982; Walker 1991;
Horak et al., 1991; Theiler 1962). Sheep and goats are also frequently
infested but their tick burdens are usually small (Fourie et al., 1988;
Fourie and Horak 1991; Horak and Fourie
1992). The preferred hosts of the immature stages of all three ticks are
scrub hares, (Horak and MacIvor 1987; Rechav et al. 1987; Horak and Fourie 1991). The immature stages of both
subspecies of H. marginatum also
infest ground-frequenting birds and those of H. truncatum infest rodents (Norval 1982; Rechav et al. 1987; Walker 1991; Horak et al. 1991).
Since the first recognised case of CCHF in
humans in South Africa in 1981 all confirmed cases have been recorded and the
actual or potential sources of infection and the localities at which infection
occurred noted. The geographic distribution of these cases has been summarised
in the same tables as the tick distribution.
Cattle, sheep, goats and large wild animals as
well as hares have been examined for ixodid ticks at several localities in
South Africa. The numbers of Hyalomma
ticks harboured by these animals are summarized in three tables, and are based
on the average numbers of ticks collected from infested animals. Where actual
numbers of ticks and animals examined and infested have been supplied in the
various publications consulted these have been used in the tables. If not these
numbers have been calculated as accurately as possible from the materials and
methods and graphic illustrations in these publications. The numbers of ticks
collected have been arranged by host and by degree of latitude from west to
east to support the gist of this communication.
A total of 158 cases of CCHF have been
diagnosed in humans in southern Africa during the 20 years since the disease
was recognised in South Africa in 1981 for the first time. One of these
infections occurred in Zaire, one in Tanzania, ten in Namibia and the rest in
South Africa. The sources and potential sources of infection for these patients
are summarized in Table 1.
|
Sources or
potential sources of human infection |
||||
|
Tick bite |
Blood or tissues
of stock or ticks |
Blood or fomites
of patients |
Lived in or
visited rural environment |
|
|
158 |
67 (42.4%) |
66 (41.8%) |
7 (4.4%) |
18 (11.4%) |
Marginally the largest group of cases (42,4%)
originated from tick bite, while a similar number (41,8%) arose from known or
potential contact with fresh blood or other tissues of livestock and/or ticks.
Most patients were employed in the livestock industry, and males constitute 129
of all cases of the disease diagnosed to date. The case fatality rate
fluctuated around 30% for the first few years after CCHF was initially
recognised in southern Africa (Swanepoel et al., 1987). It has now
declined to 23,4% (37/158), probably because greater awareness of the disease
has led to earlier recognition and better management of patients in most
instances (Swanepoel, 1994; Swanepoel, 1998; Unpublished laboratory records).
The average numbers of adult Hyalomma spp. collected from infested
cattle, zebras, gemsbok, eland and giraffes, and from smaller stock such as
sheep and goats, as well as immature ticks collected from scrub hares, and on
two occasions from Cape hares, are summarized in Tables 2-4. With the exception
of one set of sheep, no animals were examined between latitudes 21°E and 24°E.
|
Numbers of ticks collected and human cases of CCHF |
|||||
|
1621°E |
2124°E |
2427°E |
2730°E |
3033°E |
|
|
Large animals (867/1698)* |
<1 |
No
collections |
31 |
7 |
3 |
|
Sheep and goats (339/2330)* |
0 |
0 |
2 |
1 |
0 |
|
Hares (225/885)* |
0 |
No
collections |
20 |
21 |
0 |
|
CCHF cases |
10 |
24 |
46 |
21 |
10 |
* = No. infested/total no.
examined
The larger the host species the greater the
proportion infested with adult ticks and the greater the number of adult ticks
harboured. Wherever scrub hares were examined within the distribution ranges of
the ticks a large proportion of these hares were infested and the infested
animals generally had large burdens. While some H. marginatum rufipes have been recovered from eland in the arid
north-western part of the country (Table 2), none have been collected from
scrub hares or other animals in the moister, south-western region (Horak et al., 1986; Horak and
Fourie 1992; Table 1). Very few adult and no immature H. marginatum rufipes were collected from large mammals or scrub hares
respectively in the east of the country, which is generally moist and warm. The
greatest numbers of this species were encountered on the largest variety of
hosts between 24°E and 27°E. But for its southern coastal area, where no H. marginatum rufipes was recovered,
this region is considered semi-arid.
|
Numbers of ticks collected and human cases of CCHF |
|||
|
1621°E |
2124°E |
2427°E |
|
|
Large animals (27/27)* |
No
collections |
No
collections |
48 |
|
Sheep and goats (10/987)* |
1 |
1 |
No
collections |
|
Scrub hares (16/53)* |
0 |
No
collections |
167 |
|
CCHF cases |
10 |
24 |
46 |
* = No. infested/total no. examined
|
Number of ticks collected and human cases of CCHF |
|||||
|
1621°E |
2124°E |
2427°E |
2730°E |
3033°E |
|
|
Large animals (411/1725)* |
99 |
No
collections |
20 |
7 |
5 |
|
Sheep and goats (374/3041)* |
4 |
1 |
2 |
1 |
0 |
|
Hares (537/911)* |
19 |
No
collections |
50 |
27 |
53 |
|
CCHF cases |
10 |
24 |
46 |
21 |
10 |
* = No. infested/total no.
examined
With the exception of a single H. marginatum turanicum from a sheep in
the north-western region between latitudes 16°E to 21°E, and a few collected
from sheep in the south between 21°E and 24°E (Horak, and Fourie 1992), this tick was recovered only in the
Eastern Cape Province between 24°E and 27°E (Table 3). The latter collections
were all taken from wildlife in the Mountain Zebra National Park (Horak et al. 1991). This park is situated in a
semi-arid region with vegetation classified as Karroid Mountain Veld replaced
by Karoo.
Hyalomma truncatum was present on both large and small
wild and domestic animals wherever these were examined from 16°E to 30°E. The
six giraffes examined in the north-eastern regions of Mpumalanga Province were
all infested, and large numbers of immature ticks were also collected from
scrub hares in this region and in north-eastern Northern Province between
latitudes 30°E and 33°E (Table 4).
Several surveys in South Africa and Zimbabwe
during which small mammals and birds were examined, confirm that hares, and especially
scrub hares, are the preferred hosts of the immature stages of the three Hyalomma occurring in South Africa
(Norval 1982; Horak et al. 1986;
1991; Rechav et al. 1987). Wherever
immature Hyalomma of a particular
species were collected from scrub hares in the present surveys, adults of the
same species were invariably present on larger hosts (Tables 2-4).
Although the geographic distributions of the
ticks have obvious implications for the occurrence of Crimean-Congo
haemorrhagic fever, the seasonal occurrence of adult ticks is probably equally
important. Most adult H. marginatum
rufipes, H marginatum turanicum
and H. truncatum are present on
cattle or large wild herbivores from October to March.
CCHF virus has been isolated from at least 30
species of ticks, both argasids and ixodids, but only members of three ixodid
genera, namely Dermacentor, Hyalomma and Rhipicephalus have been shown to be capable of transmitting
infection transstadially and transovarially (Swanepoel 1998). However, the bulk
of the evidence suggests that Hyalomma
spp. are the principal vectors, and the known distribution of the virus broadly
coincides with the global distribution of these ticks (Hoogstraal 1956;
Swanepoel 1998). Infection with the virus is acquired by Hyalomma spp. feeding on an infected host. This could be a hare,
but possibly also a bird, in the case of the immature ticks, or a large
herbivorous mammal or an ostrich in the case of the adults (Swanepoel 1998;
Swanepoel et al., 1998). In turn these animals can themselves acquire
infection from infected ticks.
The geographic distribution of confirmed cases
of CCHF in humans is summarized with the tick numbers in Tables 2-4. The
distribution of these cases more closely corresponds to that of the two H. marginatum subspecies, and more
especially to the regions in which the heaviest concentrations of H. marginatum rufipes have been
recorded, than with the distribution of H.
truncatum. It is particularly noticeable that no human cases of CCHF have
been reported in regions south of the southern mountain ranges in the Eastern
and Western Cape Provinces, where only H.
truncatum is found and no H.
marginatum rufipes is present (Howell et
al. 1978). The prevalence of
antibodies in cattle in these southern regions was also lower than in other
parts of the country where both ticks are present (Swanepoel et al. 1987).
Although Hyalomma
ticks, their hosts and the presence of viral antibodies in the hosts are
widely distributed in South Africa the few confirmed cases of disease in humans
imply that there are barriers to infection. One of these is a difference in the
competence of the vector species, with H
marginatum rufipes being the most efficient. Another the regional abundance
of the competent vector species with the greatest numbers of Hyalomma spp., and particularly H. marginatum rufipes, present in the
semi-arid central regions of the country where human density is generally low.
A third is a low concentration of virus particles in vector adult ticks, and a
fourth the preference of these ticks for large herbivores and not for humans.
Furthermore for human infection to occur via a tick, the tick would, during its
immature stages of development, have had to feed on a hare with a sufficiently
high viral titre for it to become infected (Shepherd et al., 1989b).
Viraemia in scrub hares and rodents lasts approximately one week, but only in a
proportion scrub hares does it appear to reach an intensity sufficient to
infect feeding immature ticks (Shepherd et
al. 1989b). Viraemia in large mammals and in ostriches is also of short
duration (Shepherd et al., 1998).
The three South African Hyalomma spp. are two-host ticks. The larvae and the nymphs of H. marginatum rufipes, that together
spend about three weeks on their hosts, have a better chance of being present
on a viraemic host than the adults, that spend approximately only 10 to 14 days
on their hosts. However, the probability of a large proportion of immature or
adult ticks becoming infected from their preferred hosts is low.
Theoretically the control of H. truncatum should be less complex than
that of either of the H. marginatum
subspecies. The hare and rodent hosts of the immature stages of H. truncatum have restricted home ranges
and efficient long-term tick control on domestic livestock should
simultaneously reduce the number of immature stages on the small mammal hosts
on the same property. Although efficient long-term control on livestock will
also reduce the number of immatures of the two H. marginatum subspecies on hares and birds at the same locality,
new ticks can be reintroduced at any time by birds that have large home ranges
or are migratory.
Human infestation with Hyalomma ticks can be prevented by various precautionary measures.
Firstly these ticks are active mainly in the warmer summer months, and
particular care should be taken by hikers to regularly examine themselves for
ticks. Clothing can also be sprayed with preparations that will repel or kill
ticks. Resting or sleeping in places where large domestic or wild animals
regularly congregate is unwise as considerable numbers of adult ticks are often
present at these sites. Sleeping on the ground in summer within the
distribution range of the ticks is ill advised. Ticks should not be removed
from large stock with the naked fingers, nor should ticks be squashed between
the fingers. Particular care must be taken when performing necropsies on
recently dead large animals as Hyalomma
frequently detach from the carcass and may then reattach in the hair of the
scalp of the operator, or in the beard, if one is worn. Contact with the fresh
blood or tissues of healthy young cattle, sheep or goats during slaughter, or
that of older animals that have died from a tick-borne disease and that are
potentially coincidentally infested with CCHF infected Hyalomma spp. should be avoided by wearing gloves. Ostriches, and
if possible also cattle, destined for abattoirs should be kept free of ticks
for at least two weeks prior to slaughter.
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