Journal of General Virology (1990), 71, 1039-1043. Printed in Great Britain
1039
The effect of host resistance to tick infestation on the transmission of
Thogoto virus by ticks
Linda D. Jones and Patricia A. Nuttall*
Natural Environment Research Council, Institute of Virology and Environmental Microbiology, Mansfield Road,
Oxford OX1 3SR, U.K.
Tick-borne virus transmission was examined using
guinea-pigs and hamsters previously infested with
ticks. Guinea-pigs developed immunity to Rhipicephalus appendiculatus after a single exposure to the ticks.
Nymphal and adult stages that fed on resistant guineapigs had increased mortality during feeding, and
reduced engorged weights. Egg production from female ticks fed on resistant hosts fell by at least 50%.
Guinea-pigs maintained high levels of immunity to tick
infestation for at least 210 days after the initial
exposure. In contrast, hamsters did not develop
resistance to ticks even after three or four infestations.
R. appendiculatus adults infected with Thogoto (THO)
virus (donors) were allowed to co-feed with uninfected
nymphs (recipients) on either resistant or naive guineapigs. The number of recipient ticks that acquired virus
was significantly reduced on resistant guinea-pigs. In
contrast, feeding on pre-infested hamsters did not
affect tick-borne transmission of T H O virus. Host
resistance to tick infestation, if prevalent in nature, may
severely limit the spread of tick-borne viruses. Such an
effect could result directly from a reduction in the
number of ticks that acquire virus, or indirectly from
poor egg production (in the case of viruses maintained
in ticks by vertical transmission) and reduced survival
of ticks fed on resistant hosts.
Introduction
throughout Central Africa, and in certain areas of the
Middle East and Southern Europe, with evidence to
suggest that it is of veterinary and medical significance
(Haig et al., 1965; Moore et al., 1975 ; Davies et al., 1984).
The vector, R. appendiculatus, is a three-host ixodid tick
species endemic to most of Africa (Hoogstraal, 1956). It
is a common ectoparasite of cattle and also feeds on
sheep and goats; the larval stage is frequently found on
small rodents. R. appendiculatus is of major veterinary
and medical importance since it transmits the causative
agents of east coast fever (Theileria parva) and red water
fever (Babesia bigemina) to cattle, Nairobi sheep disease
virus (a nairovirus of the Bunyaviridae family) to sheep
and goats, and boutonneuse fever (Rickettsia conorii) to
man.
Preliminary experiments were carried out to investigate resistance to ticks in guinea-pigs and hamsters. Both
these animals serve as vertebrate hosts of THO virus in
the transmission cycle established in our laboratory
(Davies et al., 1986). Hamster develop high viraemic
titres of 7-0 to 8-0 loglo p.f.u./ml blood whereas THO
virus infection of guinea-pigs does not result in detectable viraemia ( < 20 p.f.u./ml). Nevertheless, most uninfected ticks (recipients) become infected when feeding
together with THO virus-infected ticks (donors) on
guinea-pigs (Jones et al., 1987). This form of 'non-
The effect of host resistance to feeding by larval,
nymphal or adult stages of ixodid ticks has been well
documented (Willadsen, 1980). Tick infestation of a
resistant host results in increased tick mortality during
feeding, reduced engorged weights and retarded development. Host resistance to tick infestation has an immunological basis involving complement-dependent cellular
and antibody-mediated effector mechanisms (Wikel &
Allen, 1982). The effect of host resistance to tick
infestation on the transmission of tick-borne arboviruses
has been largely unexplored. Voytakov & Mishaeva
(1980) demonstrated that animals inoculated with immune serum raised against tick salivary antigens were
protected aginst infection when exposed to ticks infected
with tick-borne encephalitis virus. Our study was
undertaken to determine the effect of naturally acquired
host immunity to tick infestation on the transmission of
Thogoto (THO) virus.
Although THO virus is structurally and morphogenetically similar to the orthomyxoviruses, it is an arbovirus
transmitted biologically by the African brown ear tick,
Rhipicephalus appendiculatus (Davies et al., 1986). The
virus was originally isolated from ticks collected from
cattle in Kenya and has subsequently been detected
0000-9028 © 1990 SGM
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1040
L. D. Jones and P. A. Nuttall
v i r a e m i c ' t r a n s m i s s i o n was used to i n v e s t i g a t e virus
t r a n s m i s s i o n i n v o l v i n g a t i c k - r e s i s t a n t host.
Table 1. Estimated yields o f eggs per female
R. appendiculatus tick f e d on either a pre-infested or a
naive guinea-pig
Methods
Cells and virus. BHK-21 and Vero cell cultures were propagated in
Eagle's medium (EMEM) supplemented with 10~ newborn calf serum
(NCS). The SiAR 126 isolate of THO virus (Albanese et al., 1972) was
obtained from Dr R. E. Shope (Yale Arbovirus Research Unit, New
Haven, Conn., U.S.A.) as an infected suckling mouse brain extract.
After selection by plaque picking three times in Vero cells, virus stocks
were derived by passage in BHK-21 cells (Davies et al., 1986).
Ticks. Larvae, nymphs and adults of R. appendicutatuswere initially
supplied by Dr M. Manhewson (Coopers Animal Health, Berkhamsted, U.K.). A laboratory colony was established by feeding the ticks on
Dunkin Hartley guinea-pigs (average weight 400 g) and maintaining
the interfeeding stages at 28 °C and a relative humidity of 85 %. Donor
ticks were infected with THO virus by feeding on viraemic hamsters
(Davies et al., 1986).
Host species. Dunkin Hartley guinea-pigs (average weight 400 g) and
DSNO strain outbred hamsters (average weight 100 g) were used
throughout the study.
Virus assay. Nymphal or adult ticks were homogenized individually
in a microtissue grinder in I ml of EMEM containing 10% NCS and
antibiotics, then clarified by centrifugation. Blood samples were
obtained by cardiac puncture from anaesthetized hamsters and guineapigs. Blood- and tick-derived materials were assayed for virus by
plaque titration in Vero cells (Davies et at., t986).
Statistical analysis. Differences between mean weights and numbers
of engorging ticks during each infestation were examined by the
Student's t-tests (P < 0.05 = significant).
Results
Acquired resistance to tick infestation by guinea-pigs
I n i t i a l studies were u n d e r t a k e n to assess the effects on
the feeding a n d d e v e l o p m e n t o f u n i n f e c t e d n y m p h a l a n d
a d u l t stages o f R. appendiculatus ticks e x p o s e d to guineapigs w h i c h h a d p r e v i o u s l y been infested w i t h ticks.
O n e g u i n e a - p i g was initially e x p o s e d to 200 larvae, a n d
a second g u i n e a - p i g to 50 n y m p h s , 33 d a y s a n d 36 days
respectively, p r i o r to a second infestation. T h e two
guinea-pigs on w h i c h ticks h a d p r e v i o u s l y fed (preinfested), a n d two g u i n e a - p i g s not p r e v i o u s l y e x p o s e d t o
ticks (naive) e a c h r e c e i v e d cohorts of 50 R. appendiculatus n y m p h s . T h e n u m b e r s o f ticks t h a t e n g o r g e d on preinfested g u i n e a - p i g s ( m e a n 8.5 + 3.5 n y m p h s ) c o m p a r e d
w i t h n a i v e g u i n e a - p i g s ( m e a n 39-5 + 6.4 n y m p h s ) , a n d
t h e i r r e s p e c t i v e m e a n weights o f 4-2 + 1.3 m g a n d
9.2 + 2 . 0 mg, were significantly r e d u c e d ( t = 6 . 0 2 2 ,
7.690; P < 0.05, < 0.001, respectively). T h e r e was no
difference in the t i m e t a k e n to engorge (6 to 8 days) or the
n u m b e r o f e n g o r g e d ticks t h a t s u b s e q u e n t l y m o u l t e d to
adults, a l t h o u g h e m e r g e n t adults d e r i v e d f r o m preinfested hosts were s m a l l e r (male 1.6 + 0-6 mg, f e m a l e
1.4 + 0-5 m g t h a n those fed o n n a i v e hosts (male 4-2 +
1-1 mg, f e m a l e 3-8 + 0.6 mg).
Tick
no.
Host
status*
Engorged weight
of female tick
(mg)
Total no.
eggs laidt
Weight
of female
(mg):~
5-1
5-2
5-4
6-1
6-2
6-3
6-5
6-6
6-7
6-8
6-9
6-11
6-12
6-13
+
+
+
-
73.7
77.3
98.5
341.0
270.8
348-2
173-0
293.1
282.0
202.8
312.6
262.0
218.5
214-1
435
506
576
2419
1767
1995
1167
1923
1686
1270
1996
2125
1592
1554
37-0
18-2
20-0
186-2
132.5
207-4
100-0
161-3
158-I
105.8
125.1
104.4
96.5
126.0
* +, Pre-infested guinea-pig (previously exposed to 200 larvae, 27
days prior to reinfestation with adult ticks); - , naive guinea-pigs (not
previously exposed to ticks).
t Eggs collected over a 10 day period after commencement of
oviposition. Batches of 100 eggs from ticks fed on the pre-infested or
naive hosts were weighed at each collection. The numbers of eggs per
female were estimated from these weights.
:~Female weighed at end of 10 day oviposition period.
I n a second e x p e r i m e n t , a p r e - i n f e s t e d a n d a n a i v e
g u i n e a - p i g were e a c h infested w i t h 32 R. appendiculatus
adults (equal sex ratio). T h e r e was no significant
difference in the n u m b e r o f ticks t h a t e n g o r g e d (preinfested, 9/16 f e m a l e a n d 14/16 m a l e ; naive, 13/16
female a n d 13/16 male). T h e t i m e t a k e n to c o m p l e t e
e n g o r g e m e n t was longer on the p r e - i n f e s t e d host,
r a n g i n g from 11 to 18 days, c o m p a r e d w i t h 9 to 12 d a y s
on the n a i v e host ( t = 11-555; P < 0-001). T h e m e a n
w e i g h t o f e n g o r g e d females (42.7 + 40.5 mg) on the preinfested host was significantly r e d u c e d c o m p a r e d w i t h
t h a t on the n a i v e host (268-4 +_64.0 rag, females)
( t = 8.07; P < 0 . 0 0 1 ) ; the m a l e s h a d s i m i l a r weights
(63.4 _+ 13.7 mg, pre-infested host; 63.6 +_ 12.8 mg, n a i v e
host). T h e egg yield p e r f e m a l e tick was e s t i m a t e d o v e r a
10 d a y p e r i o d starting at c o m m e n c e m e n t o f oviposition.
O f the nine females fed on the p r e - i n f e s t e d host, six failed
to p r o d u c e eggs c o m p a r e d w i t h two o f 13 on the n a i v e
host. Egg p r o d u c t i o n f r o m females fed on the preinfested host was r e d u c e d by at least 5 0 ~ ( T a b l e 1).
T H O virus transmission on guinea-pigs resistant to tick
infestation
A total o f 16 to 20 adult R. appendiculatus t i c k s i n f e c t e d
w i t h T H O virus (donors) was p l a c e d in one c h a m b e r , a n d
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Transmission o f Thogoto virus by ticks
1041
Table 2. Effect of host resistance to tick infestation on the ability of R. appendiculatus nymphs to acquire
Thogoto virus
Female donor ticks*
Recipient ticks
Guinea-pigs
No.
Status't
Day:~
Percentage
fed
Mean weight (mg)
(range)§
Percentage
fed
Mean weight (mg)
(range)
Percentage
virusll
G10
GI1
G12
G13
G16
GI7
GI8
G7
G8
G9
GI4
G15
+
+
+
+
+
+
+
-
33
33
58
58
191
197
210
0
0
0
0
0
90
60
63
63
100
100
75
90
90
88
100
100
22.4 (2-9-68.2)
12.9 (3-1-28.7)
27-1 (1-7-52-0)
15.2 (3.0-30.4)
49.3 (19-8-68.0)
49-3 (3.12-68-0)
21.2 (2.3-41-5)
23.7 (3.5-49.8)
26.4 (3.2-85-8)
47.3 (3-940.3)
85.3 (70.1-99.4)
71.9 (44-2-91-6)
28
20
40
4
64
20
56
42
60
70
94
94
4.2 (2.1-6.4)
2.6 (1.2-4.9)
3-6 (l-5-6.9)
3-4 (2.0-4.8)
2.9 (1.1-7-1)
2.4 (1.3-3.1)
3.0 (0-9-6-5)
8.5 (7.0-10-5)
8.2 (6.3-10.0)
8.6 (4-9-12.0)
10.7 (7-4-13.1)
10.3 (7.9-12.4)
14
10
40
50
0
0
10
85
75
90
80
85
* Donor ticks were infected by feeding at the nymphal stage on viraemic hamsters (Davies et al., 1986).
1"See Table 1".
Number of days following the previous tick infestation.
§ Female ticks were weighed on the day of detachment of nymphs and were not replete.
IIIndividual nymphs were homogenized and assayed for virus on day 12 post-engorgement (the time of maximum virus titre).
Table 3. Thogoto virus transmission by R. appendiculatus
nymphs* to either pre-infested or naive hamsters
Hamster
No.
H5
H6
H7
H8
H1
H2
H3
H4
Status:~
+
+
+
+
-
Virus titre
(loglo p.f.u./ml at h)t
No. of
infestations
48
72
96
3
3
2
2
0
0
0
0
7-0
0
3-9
4.1
6-4
4.5
2-5
6.4
D§
5.9
6-9
6.3
7.6
7.5
8.0
7.8
7.4
8-3
7.2
D
D
D
D
120
* Nymphs were infected by feeding at the larval stage on viraemic
hamsters (Davies et al., 1986).
t Virus titre/ml hamster blood at various times post-attachment of
infected ticks.
See Table 1".
§ D, Dead.
cohorts o f 50 u n i n f e c t e d n y m p h s (recipients) were p l a c e d
in a s e p a r a t e c h a m b e r on e a c h o f 12 g u i n e a - p i g s (G7 to
G 18; T a b l e 2). F o l l o w i n g r e p l e t i o n o f r e c i p i e n t n y m p h s ,
79 ~o female d o n o r ticks h a d p a r t i a l l y e n g o r g e d on preinfested g u i n e a - p i g s a n d 94 ~ on n a i v e guinea-pigs, with
m e a n weights o f 28.2 + 15.2 m g a n d 50.9 _+ 27-3 mg,
respectively. F e m a l e d o n o r ticks r e c o v e r e d f r o m preinfested g u i n e a - p i g s h a d a m e a n virus titre o f 3-8 log~o
p.f.u./tick, a n d 4.1 log~0 p . f . u . / t i c k on n a i v e hosts.
T h e m e a n n u m b e r s o f r e c i p i e n t n y m p h s t h a t fed on
p r e - i n f e s t e d c o m p a r e d w i t h n a i v e hosts (16.6 + 10.7 a n d
36.0_+ 11.2, respectively) a n d t h e i r m e a n weights
( 3 - 2 + 0 - 6 m g a n d 9.3-+ 1.2 mg, respectively) were
r e d u c e d ( t = 3 . 0 4 2 , 19.543; P < 0 - 0 2 ,
<0.001). Only
15/116 (13 ~ ) e n g o r g e d r e c i p i e n t n y m p h s a c q u i r e d virus
w h e n fed on pre-infested g u i n e a - p i g s ( m e a n o f 2-1 -+ 2-8
ticks p e r a n i m a l ) c o m p a r e d w i t h 149/180 (83 ~ ) t h a t fed
on n a i v e hosts ( m e a n o f 29.8 + 9-7 ticks p e r a n i m a l )
( t = 7.153; P < 0.001). T h e r e was no significant difference in e i t h e r the virus titres o r t i m e t a k e n to e n g o r g e (6
to 8 days) b e t w e e n the two groups.
Thogoto virus transmission on hamsters previously
exposed to tick infestation
F o u r h a m s t e r s (H5 to H 8 ; T a b l e 3) e x p o s e d to two or
three tick i n f e s t a t i o n s (by 200 l a r v a e o r 50 n y m p h s ) d i d
n o t d e v e l o p resistance to ticks. T h e r e was no significant
difference b e t w e e n p r e - i n f e s t e d a n d n a i v e h a m s t e r s in
e i t h e r the n u m b e r o f ticks w h i c h f e d at each i n f e s t a t i o n
( m e a n o f ticks, p o s t - s e c o n d i n f e s t a t i o n w i t h n y m p h s :
35.3 +__11.4 a n d 34.8 + 10.7, r e s p e c t i v e l y ; p o s t - t h i r d
i n f e s t a t i o n w i t h n y m p h s ' 38.5 + 0.7 a n d 42.5_+ 4.9,
respectively), or t h e i r m e a n b o d y weights (post-second
i n f e s t a t i o n : 6.1 +_ 1.8 m g a n d 5.2 + 1.6 mg, r e s p e c t i v e l y ;
p o s t - t h i r d i n f e s t a t i o n : 5.2 + 1.5 rng a n d 5.2 + 1.7 mg,
respectively).
P r e - i n f e s t e d (H5 to H8) a n d n a i v e (H 1 to H4) h a m s t e r s
were e a c h infested w i t h cohorts o f 50 T H O v i r u s - i n f e c t e d
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1042
L. D. Jones and P. A. Nuttall
nymphs (Table 3). All the hamsters became infected with
THO virus. The replication time of the virus and
maximum virus titre were not significantly different for
pre-infested and naive hamsters.
Discussion
The control of ticks by conventional methods such as
spraying or dipping can be environmentally hazardous.
In addition, these methods may have a short-lived effect
owing to development of tick resistance to acaricides
(Drummond, 1970). Induction of host immunity to tick
infestation represents an alternative approach to the
control of ticks and the pathogens they transmit (Allen &
Humphreys, 1979; Wikel, 1980, 1981).
Several reports indicate that resistance to ticks may
affect the transmission of tick-borne agents. Transmission of Babesia argentina and B. bigemina to cattle
resistant to tick infestation was greatly reduced compared with infection of susceptible cattle (Francis &
Little, 1964), and host resistance adversely affected
transmission of the tick-borne bacterium Francisella
tularensis to tick-resistant hosts (Bell et al., 1979). Tickresistant oxen showed a mild response to infection with
tick-transmitted Theileria parva whereas the infection in
naive oxen was fatal or severe (Fivaz et al., 1989). In
contrast, infections of cattle with B. boris resulted in
immunosuppression of the host which interfered with the
immune resistance mechanism to the tick vector, thus
leading to a greater susceptibility to disease (Callow &
Stewart, 1978). Similarly, infection of rabbits with
Trypanosoma congolense blocked the expression of
immunity in tick-resistant hosts (Heller-Haupt et al.,
1983). In this paper, we have investigated THO virus
transmission involving guinea-pigs and hamsters that
had previously been infested by R. appendiculatus ticks.
A single infestation with ticks was sufficient to confer
resistance in guinea-pigs which lasted for at least 210
days. On tick-resistant guinea-pigs, the numbers of
nymphs that successfully fed and their engorged weights
were reduced; there was no apparent effect on the
numbers that moulted, although emergent adult ticks
(from nymphs that fed on resistant hosts) were undersized. The effect of host resistance on tick-feeding and
development was the same irrespective of whether the
ticks were infected by THO virus. Similarly, there was no
evidence that virus infection of guinea-pigs (presumed to
occur during non-viraemic transmission; Jones et al.,
1987) affected the expression of tick resistance since
recipient ticks performed the same when co-feeding with
either infected or uninfected ticks. However, virus
acquisition by uninfected ticks was greatly reduced on
tick-resistant guinea-pigs.
On resistant guinea-pigs only 4 % (15/350) of recipient
nymphs became infected compared with 69% (149/250)
on naive hosts. This reduction in the number of ticks
infected was partly because fewer ticks fed on the
resistant hosts. Nevertheless, of the recipients that
engorged, only 13~ became infected compared with
83% on naive hosts. Several factors may account for the
decrease in incidence of infection of ticks fed on resistant
hosts: (i) reduced virus intake since blood meal sizes
were smaller; (ii) a decrease in the amount of virus
infecting the guinea-pigs resulting from partial inhibition of feeding by infected adult ticks (although the
number of engorged adult donors was unaffected); (iii)
'resistance factors' in the blood of guinea-pigs that
directly or indirectly inhibited virus infection of ticks.
Evidence that virus infection of ticks is inhibited by a
blood meal from a resistant host has not been accrued.
However, ticks fed on resistant hosts have been reported
to show signs of pathological degeneration of the gut cells
(Walker & Fletcher, 1987). Such an effect in the gut
could provide a hostile environment for infecting virus.
Apart from the direct evidence presented above, that
THO virus transmission is adversely affected by feeding
on tick-immune hosts, several other observations have
significance for the epidemiology of tick-borne viruses.
First, adults moulted from nymphs that had fed on
resistant guinea-pigs were undersized. Undersized ticks
have a reduced capacity for survival in nature (Chiera et
al., 1985). The chances of such ticks transmitting virus
would be reduced accordingly. Second, fewer adult
female ticks laid eggs after engorging on tick-resistant
guinea-pigs. The lower numbers of eggs produced
reflected the reduced blood meal size of females that
oviposited (Gray, 1981). Chiera and colleagues (1985)
showed that the cumulative effects of three successive
resistant hosts in the life-cycle could result in ticks failing
to produce eggs. They suggested that a high level of
resistance in the vertebrate host population could shift
the tick-host equilibrium to a lower level by virtue of
reduced tick egg production and survival. The cumulative effect of host resistance could be deleterious to the
survival of tick-borne arboviruses in the field, especially
those viruses that are maintained in ticks by vertical
transmission (Tesh, 1984).
In contrast to guinea-pigs, hamsters did not develop
resistance to R. appendiculatus ticks even after repeated
infestations with larvae or nymphs. Similar observations
have been reported for deer mice infested with Dermacentor variabilis (Trager, 1939), Apodemus sylvaticus with
Ixodes trianguliceps (Randolph, 1979), and dogs with R.
sanguineus (Chabaud, 1950). Also, there was no evidence
that pre-infestation influenced the infection of hamsters
exposed to THO virus-infected ticks. Thus, although the
induction of host immunity to tick infestation may
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Transmission of Thogoto virus by ticks
provide some level of protection against tick-borne
viruses, not all animals will necessarily become immune
to ticks.
The authors wish to thank M. L. Hirst and E. Hodgson for help with
the ticks, J. S. Cory for statistics and D. H. L. Bishop for support.
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(Received 20 April 1989; Accepted 10 January 1990)
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