Download Infestation in the dog by the paralysis tick 2

the ticks were rapidly engorging. The duration of the disease
was variable, although as found by Ross (1927) those dogs
which showed earliest clinical signs tended to deteriorate more
rapidly than dogs with later onset of signs. This became more
obvious in later studies and may explain why some dogs, even
though presented to veterinarians early in the disease, die
quickly despite treatment, while other animals presented later
in the disease recover.
The main clinical signs observed in this experiment were
consistent with a rapidly ascending flaccid motor paralysis
and similar to those documented by Dodd (1921), Ross (1926)
and Knott (1961). Division of the disease into different stages
based on clinical signs has been described by Hindmarsh and
Pursell (1935) and Furneaux (1969). However these were not
considered detailed enough to use in future investigations,
necessitating accurate documentation of the clinical signs of
the disease.
The progressive reduction in awareness to painful stimuli
suggested some involvement of the sensory pathways. This
loss of sensation has not been reported previously; in fact
Dodd (1921), Ross (1926) and Hamilton (1940) all report that
the integrity of the afferent pathways was maintained. Although present in all dogs in this experiment, sensory loss was
not a consistent feature in further experiments; however its
presence in this study means that it could be a feature of tick
paralysis in some cases.
A detailed neurological examination was not carried out;
however, the withdrawal reflex, gag reflex and pupillary reflex
were examined. The diminished response and final loss of the
withdrawal reflex could result from a lesion anywhere along
the reflex arc and Cooper (1976) has demonstrated failure of
acetylcholine release at the neuromuscular junction. Cranial
nerve involvement was indicated by pupillary dilation which
could result from either paralysis of the oculomotor nerve as
postulated by Cooper (1976) or stimulation of the cervical
sympathetic nerve. The diminished gag reflex indicated in-
volvement of the autonomic nervous system with paresis of
the glossopharyngeal and vagus nerves and highlighted the
importance of “nil by mouth” in all dogs with tick paralysis.
Microscopic findings of congestion and focal haemorrhages
in the brain and spinal cord have been reported by Ferguson
(1924), Ross (1926), Cooper (1976) in tick paralysis.
The finding of pulmonary congestion and in some cases
pulmonary oedema was unexpected as although it has been
reported previously (Ross 1926; Hindmarsh and Pursell 1935;
Calder 1974; Cooper 1976) it has not been emphasised as an
important aspect of tick paralysis. From this study the cause
could not be determined; however, it was felt that it probably
contributed to death.
In summary, under laboratory conditions the disease produced by Ixodes holocyclus in the dog has a variable onset
and duration. The clinical signs indicated that the most prominent neurological disturbance was in the efferent motor system; however, the afferent pathways as well as the autonomic
nervous system were also involved. Pulmonary congestion
and/or oedema was a consistent post-mortem finding.
References
Calder, M (1974) - Control and Therapy No. 233, 102. (Post-Graduate Committee in Veterinary Science, University of Sydney)
Cooper, BJ (1976) - Studies on the Pathogenesis of Tick Paralysk
PhD Thesis, University of Sydney.
Dodd, S (1921) - J Comp Path 34: 309
Ferguson, E W (1924) - Med J Aust 2: 346
Furneaux, R W (1969) - Control and Therapy in General Practice
No 31, I (Post-Graduate Committee in Veterinary Science, Uni-
versity of Sydney)
Hamilton, D G (1940) - Med J Aust 1: 759
Hindmarsh, W L and Pursell, R T (1935) - Aust Vet J 11: 229
Knott, S G (1961) - Qd Agric J 87: 41
Ross, I C (1926) -Parasitology 18: 410
Ross, I C (1927) - Aust Vet J 19: 71
(Accepted for publication 12 November 1986)
Infestation in the dog by the paralysis tick Ixodes hoZocycZus
2. Blood-gas and pH, haematological and biochemical findings
J E ILKIW and D M TURNER*
Department of Veterinary Clinical Studies, University of Sydney, New South Wales 2006
SUMMARY: Arterial blood-gas and pH, haematological and biochemical estimations
were carried out on 8 dogs infested with lxodes holocyclus and 2 uninfested controls.
The arterial blood-gas and pH measurements did not change significantly until the
dogs were recumbent and unable to lift their heads. When affected dogs became
moribund, moderate hypoxaemia with acute ventilatory failure was present. The
significant haematological and biochemical abnormalities were difficult to interpret
individually, but taken together could reflect sympathetic stimulation of the adrenal
cortex or medulla.
Aust Vet J 64: 139-142
Introduction
Since dogs with Ixodes holocyclus toxaemia show characteristic signs, aids to diagnosis are rarely utilised by veterinarians and therefore little information is available about the
laboratory changes.
The present experiment was undertaken to document the
changes in blood-gas and acid-base, haematological and biochemical values in dogs where the disease was produced in
the laboratory by attachment of adult female Ixodes holocvclus.
The Forest Animal Hospital, 61 2 Warringah Rd, Forestville,
New South Wales 2087
Australian Veterinary Journal, Vol. 64, No. 5, May, 1987
Materials and Methods
Ten healthy cross-bred dogs, 5 males and 5 females, ranging
from 20.7 to 32.0 kg were used in this study. The dogs were
randomised and 2 dogs not infested served as controls. One
week prior to attachment of the ticks, the dogs were surgically
prepared by implantation of a catheter in the carotid artery
to enable collection of arterial blood.
Arterial blood-gas and pH, haematological and biochemical
estimations were carried out on all dogs on the 2 days preceding attachment of the ticks to provide baseline control
data.
The partial pressure of oxygen ( P k J and of carbon dioxide
(Pacoz) in arterial blood measured in millimetre of mercury
139
(mmHg), and the pH of the arterial blood were measured
electrometrically with a blood-gas analyser, BMS 3.t
The span of the pH electrode was calibrated with precision
buffer solutions S1500 and S1510 while the carbon dioxide
and oxygen electrodes were calibrated with gases of known
concentrations. t
The calibrations were checked twice weekly against known
gas and pH concentrations.$ A 2 ml sample of blood was
collected anaerobically over a period of 15 seconds into a
glass syringe, the deadspace of which was filled with 1:lOOO
international units per millilitre of heparin, and analysis performed immediately. All measurements were made at 37OC
and the results were corrected for body temperature (Temp),
using a blood-gas calculator, BGCl .t Standard bicarbonate
(Std HCO, in millimoles per litre, mmo1.L-') was calculated
using the blood-gas calculator.
Haematological estimations were carried out on 2.5 ml of
blood collected into a tube containing dipotassium ethylenediamine tetra-acetate as anticoagulant. Packed cell volume
(PCV), total plasma protein (TPP), haemoglobin (Hb), total
red blood cells (RBC) and total white blood cells (WBC) were
measured. Haemoglobin (grams per litre, g.L-') was estimated
by the cyan-methaemoglobin method. Total red blood cells
(xl0" per litre, x1012.L-1)and white blood cells (x109.L-') were
counted using an electronic counter.§ Packed cell volume (litre
per litre, L.L-') was determined by the microhaematocrit
centrifuge technique and total plasma protein (g.L-') measured
using a refractometer.1
Biochemical estimations were carried out on plasma obtained by spinning 10 ml of heparinised blood at 2000 g for
5 min. Measurements of sodium (Na, mmo1.L-I), potassium
(K, rnmo1.L-I), phosphate (PO,, mmo1.L-I), total protein
(TP, g.L-'), albumin (ALB, g.L-'), total carbon dioxide
(TCO,, mmo1.L-I), urea (U. mmol.L-'), cholesterol (CHOL,
mmo1.L-I), glucose (GLUC, mmo1.L-'), total bilirubin (TBIL,
micromole per litre, umo1.L-') and alkaline phosphate (AP,
units per litre u.L-') were made using an autoanalyser# and
standard Technicon 12/60 methods. Calcium (Ca, mmol.L-')
and magnesium (Mg, mmo1.L-') were determined using a
spectrophotometer** with lanthanium as diluent and creatine
phosphokinase (CPK, u.L-') by the Rosalki ultraviolet kinetic
method.
Four ticks were attached to 6 of the dogs, while 2 dogs
were infested with 3 ticks. Two dogs not infested with Ixodes
holocyclus served as controls to enable between-dog and between-day variations in the measurements throughout the experimental period to be documented.
In the 2 dogs that were not infested arterial blood was
collected for all determinations on days 2, 4 and 8 of the
experimental period. Additional samples were taken on day 6
for blood-gas and pH measurements and on days 1 and 6 for
biochemical estimations.
In the tick-infested dogs, blood was collected for the various
estimations on alternate days until signs of the disease were
observed. Once signs were evident blood was collected at the
various stages of the disease as described by Ilkiw et a1 1987
and outlined below:
Stage I - the dogs showed paresis when walked
Stage 2 - the dogs were unable to stand but could right
Stage 3 - the dogs were unable to right
Stage 4 - the dogs lacked limb withdrawal reflexes
Stage 5 - moribund
t
Radiometer A/S, 45 Booralie Road, Terrey Hills, New South
Waies
$ Versatol Acid Base, General Diagnostics, Caringbah, New
South Wales
Coulter Counter Model F, Coulter Electronics Ltd, Luton,
United Kingdom
1 Series PRB, American Optical Company, Keene. United
States of America
# S M A 12/60, Technicon Equipment Pty Ltd, North Ryde,
New South Wales
303, Perkin-elmer Pty Ltd, Milperra, New South Wales
140
A two-way analysis of variance as described by John and
Quenouille (1977) was carried out on the measurements obtained from the 2 control dogs throughout the experimental
period.
The results of the blood-gas, pH and biochemical measurements were analysed by pairing the control and test values
in each animal, and the mean differences at each stage were
compared with zero using the Student's t-distribution. Simple
logarithmic transformations were carried out on the data of
glucose, cholesterol and creatine phosphokinase at all stages
of the disease, because these values were distributed over a
very wide range. The transformed data were then analysed by
a Student's t-test.
The results of the haematological measurements were analysed by pairing the control and test values in each animal,
and the mean differences at stage 5 of the disease compared
with zero using the Student's t-distribution.
Results
Arterial Blood-gas and pH, Haematological and Biochemical
Measurements in Control Dogs throughout the Experimental
Period
There were no significant changes in arterial oxygen tension,
arterial carbon dioxide tension, pH and standard bicarbonate
between dogs or between sampling times. However, temperature showed a significant variation between dogs. Haematological examination revealed no significant changes between
dogs or between sampling times.
Within the biochemical values calcium and phosphate
showed both between-dog and between-sampling-time variations. Alkaline phosphatase and creatine phosphokinase
showed only between-dog variations, while potassium, total
carbon dioxide and total bilirubin showed only between-sampling-time variation.
Arterial Blood-gas and p H Measurements during the
Disease
Arterial oxygen tension, arterial carbon dioxide tension,
pH, standard bicarbonate and temperature at the control
period and at the various stages of the disease are shown in
Table 1.
At stages 1, 2 and 3 there were no significant changes in
values from control.
For stage 4 there was a significant elevation in arterial
carbon dioxide tension, while arterial oxygen tension, pH,
standard bicarbonate and temperature remained unchanged.
During stage 5 all values except temperature showed significant changes from control. Arterial oxygen tension, pH
and standard bicarbonate fell significantly, while arterial carbon dioxide tension rose significantly.
Haematological Measurements during the Disease
The change in haematological values between control data
and dogs at stage 5 is shown in Table 2.
Haemoglobin rose significantly, while all other values showed
no significant change.
Biochemical Measurements during the Disease
The differences from control in biochemical values at the
various stages of the disease are demonstrated in Table 3.
During stage 1 protein rose significantly from control. The
other measurements did not change significantly. During stage
2 potassium, albumin, urea and total bilirubin fell significantly, while glucose and cholesterol rose significantly above
control values. There was no significant difference from control in the other measurements. At stage 3 there were significant falls in potassium, total carbon dioxide, urea and
total bilirubin, while glucose and cholesterol were significantly
elevated from control. The other measurements did not change
significantly. At stage 4 significant falls were found in potassium and urea, while glucose and cholesterol rose significantly
from control. There were no significant differences for the
other measurements. At stage 5 phosphate, cholesterol, glucose
Australian Veterinary Journal, Vol. 64, No. 5 , May, 1987
TABLE 1
Changes in arterial blood-gases and pH measurements at the various stages of paralysis caused by lxodes holocyclus
Control
Paon
pacon
mmHg
mmHg
PHa
Std.HC0,
Temp
*
rnmol.L-'
"C
Stage 1
paresis
Stage 2
unable to walk
Stage 3
unable to right
MeanfSem
MeankSem
Mean+Sem
MeankSem
Stage 4
Stage 5
unable to right moribund
and lacking limb
withdrawal
reflexes
MeanfSem
MeanfSem
n=10
n=4
n=4
n=4
n=4
n=5
92.22 f 1 . 6 3
30.78 f o . 9 8
7.36a+o.ooa
19.61 50. 47
38.61 f 0 . 1 6
97.45 23.69
25.40 f 2 . 4 5
7.395+0.035
19.20 f0.87
38.70 f o . 1 1
88.13 f 1 . 6 4
31.73 22.45
7.378fo.010
20.08 20.45
38.58 20.06
89.88 22.73
31.00 21.83
7.39ofo.01 1
19.98 20.20
38.38 f0.21
74.47 55.26
38.84 f4.75'
7.3iafo.016
19.75 20.78
37.92 f 0 . 2 1
55.64 f 5 . 9 7 * * *
51.36 ?3.35***
7.203+0.0i5**
17.74 r0.54""
37.16 f i . 0 1
p<0.05
* * * p<O.Ol
TABLE 2
Changes in haematological values in dogs paralysed by
lxodes holocyclus
Control
MeankSem
Stage 5
moribund
MeankSem
n = 10
n = 5
PCV L.L-'
TPP g.L-'
Hb g.L-'
RBC xl O'*.L-'
WBC X I O ~ . L - ~
0.46k0.01
67.8 k l . l
147. 1 f 3 . 4
6.36f0.16
1 5.38k 1 . 1 5
0.50k0.02
75.8 f 4 . 3
166.8k7.7'
6 . 8 0 f0.30
20.82k4.84
*p<0.02
and creatine phosphokinase rose significantly, while total
bilirubin fell significantly. The other measurements did not
differ significantly from control.
Discussion
Analysis of the various measurements in the control dogs
revealed significant between-sampling-timevariations in serum
levels of potassium, calcium, phosphate, total carbon dioxide
and total bilirubin. Changes in these measurements at the
various stages of the disease, when within the normal range,
were probably due to day-to-day variations and were unlikely
to be of clinical significance.
Although 8 dogs were infested with ticks only 7 dogs showed
clinical signs and because of the rapid development of the
disease in some animals not all measurements were taken.
Arterial blood-gas and pH measurements in cases of tick
paralysis have not been documented previously. Measurements
of these indices indicated that there was no significant change
from control until the fourth stage of the disease. The elevation
in arterial carbon dioxide tension in stage 4, although significant, is not physiologically important as it is within the
normal range for the dog (Feigl and D'Alecy 1972). From this
point until death the dogs showed a progressive decrease in
ventilatory capacity, with moderate hypoxaemia and acute
ventilatory failure. A mild non-respiratory acidosis was also
present.
While this experiment demonstrated that ventilatory failure
occurred in the late stages of the disease, the cause was unclear.
Although respiratory muscle paralysis (Hamilton 1940; Roberts 1941, McCarthy 1958) has been blamed for death in this
disease, the dogs in this experiment appeared to be making
considerable respiratory effort during the stages when bloodgas analysis showed ventilatory failure to be developing. Moist
rales and post-mortem changes suggestive of pulmonary
congestion and oedema were also found (Ilkiw et a1 1986) and
could have contributed to the respiratory failure.
Haematological measurements in animals with tick poisoning have not been described previously. The changes encountered here were minor. The significant increase in haemoglobin
concentration could possibly be due to mild dehydration as
TABLE 3
Changes in biochemical values at the various stages of paralysis caused by lxodes holocyclus
Na
K
Ca
Mg
PO,
TP
ALB
TCO,
U
CHOL
GLUC
AP
TBlL
CPK
'
t t
It,
***t
mmol.L-'
mrno1.L-'
mmo1.L-'
mmo1.L-'
mmol.L-'
g.L-'
g.L-'
mmo1.L-'
mmol.L-'
mmo1.L-'
mmol.L-'
u.L-'
pinol.L"
u.L-'
Control
Stage 1
paresis
Stage 2
unable to walk
Stage 3
unable to right
MeankSem
MeankSem
n = 4
MeanfSem
n = 4
mean+Sern
n = 10
146.6 f
4.51 f
2.61
0.77 f
1.32 f
65.5 f
29.4 f
20.96 f
6.50 f
4.79 f
6.13 f
52.8 f
5.81 k
22.3 f
0.4
145.5 f 1.3 146.3 f 0.5
0.07
4.48 f 0.11 3.90 f 0.12**
0.01
2.59 f 0.04 2.53 f 0.02
0.02
0.75 f 0.04 0.71 f 0.02
0.04
1.28 f 0.10
1.53 f 0.15
0.7
67.8 f 2.0' 66.3 f 0.9
0.4
29.5 f 1.2 27.3 f 1.0"
0.77 15.32 f 1.92 17.18 f 0.39
0.50
4.21 f 0.36 3.57 f 0.39'
0.20
5.11 f 0.14 5.61 f 0.51"
0.14
6.24 f 0.52 6.99 f 0.03"'
6.7
63.8 f 16.9 82.3 f 14.8
0.17
3.42 f 0.00""
3.93 k 0.51
1.9
19.3 & 5.3 27.3 f 4.8
n = 4
146.3 f
4.08 f
2.53 f
0.71 f
1.43 f
66.8 f
28.3 f
17.40 f
3.50 f
5.14 f
6.56 f
64.3 f
2.56 f
57.8 f
0.6
0.14"
0.08
0.03
0.14
1.3
1.7
0.73"'
0.46"
0.24
0.24"
19.6
0.51""
35.0
Stage 4
unable to right and
lacking limb
withdrawal reflexes
MeankSem
n = 4
144.5 f
3.83 f
2.55 f
0.79 f
1.82 f
69.8 f
28.3 f
19.70 f
4.46 f
6.99 f
9.94 f
58.3 f
2.22 ?
22.8 f
0.9
0.13"
0.05
0.08
0.1 1
3.9
1.3
0.80
0.50'
1.00"'
2.41 * * *
7.6
1.03
5.7
Stage 5
moribund
Meanf Sem
n = 5
144.0 f 2.6
4.04 f 0.40
2.60 f 0.07
0.92 f 0.12
2.23 f 0.12"'
74.6 & 4.8
29.8 f 1.6
17.86 f 0.99
4.86 f 0.79
6.85 f 0.82'
11.26 f 2.64'
64.8 f 8.8
1.71 f 1.03'
223.0 f 152.4"'
p<0.05
p < 0.02
p<o.o1
p < 0.001
Australian Veterinary Journal, Vol. 64, No. 5 , May, 1987
141
the total red cells, plasma protein and packed cell volume
demonstrated similar, although insignificant, elevations. Dehydration would be expected in animals which were not drinking or eating and had been vomiting however it is important
to note that if present in tick paralysis it is only mild. Fluid
therapy is therefore not usually needed and because pulmonary
congestion is present, may be contraindicated. Haematological
changes in man also appear to be mild. Pearn (1966) reported
the haematological picture in a child with tick paralysis and
associated myocarditis where the indices measured were within
the normal range, but the neutrophils showed mild toxic
changes.
It was anticipated that few biochemical values would be
altered in this disease. However, since these indices have not
been measured previously, it was thought that detailed investigation should be performed to establish what changes, if
any, occur. Many of the significant changes in these measurements are difficult to interpret individually, but viewed
together they could represent the biochemical response to
sympathetic stimulation of the adrenal medulla, causing release
of adrenaline and nor-adrenaline or release of adrenocorticotrophic hormone, resulting in stimulation of the adrenal
cortex to secrete corticosteroids. Release of any of these hormones could cause the elevations in glucose, cholesterol and
haemoglobin, as well as the fall in potassium (Goodman and
Gilman 1975).
Although phosphate showed a time variation in the control
dogs the elevation in the tick infested dogs at stage 5 was
physiologically abnormal. Severe muscle cell damage, with
liberation of phosphate into the blood, could explain the
elevated level (W Hensley, personal communication). Active
muscle cell lysis was also suggested by the elevation in creatine
phosphokinase. An elevation in creatine phosphokinase was
reported in a case of tick paralysis caused by the American
tick, Derrnacentor andersoni, and it was thought that the tick
toxin caused muscle damage by interference with cellular energy metabolic pathways (Boffey and Paterson 1973).
In summary, laboratory changes in dogs with tick paralysis
were minimal until an advanced stage of the disease was
reached. Dehydration was mild, but acute ventilatory failure
and a mild non-respiratory acidosis were present. Muscle damage also appeared to occur.
References
Boffey, G C and Paterson, D C (1973)-Can Med Ass J 108: 866
Feigl, E 0 and D’Alecy, L G (1972)-J Appl Physiol32: 152
Goodman, L S and Gilman, A (1975)-The Pharmacological Basis
of Therapeutics,Macmillan Publishing Company Incorporated, New
York
Hamilton, D G (1940)-Med J Aust 1: 759
Ilkiw, J E, Turner, D M and Howlett, R C (1987)-Aust Vet J 64:
137
John, J A and Quenouille, M H (1977)-Experirnents: Design and
Analysis Charles Griffin and Company Ltd, London
McCarthy, P H (1958)-Qd Agric J 84: 230
Pearn, J H (1966)-Med J Aust 1: 629
Roberts, F H S (1941)-Qd Agric J 67: 189
(Accepted for publication 12 November 1986)
Infestation in the dog by the paralysis tick Ixodes holocyclus
3. Respiratory effects
J E ILKIW and D M TURNER*
Department of Veterinary Clinical Studies, University of Sydney, New South Wales 2006
SUMMARY: To assess respiratory function in dogs with tick paralysis, respiratory
measurements were recorded on 14 dogs experimentally infested with lxodes holocyclus.
There was a progressive fall in respiratory rate with no change in tidal volume, which
resulted in a significant fall in minute respiratory volume in the latter stages of the disease.
The fall in respiratory rate was possibly central in origin and was accompanied by an
increased alveolar-arterial oxygen tension difference, probably caused by pulmonary
congestion and oedema. The “grunting” respiration seen in tick paralysis was due to closure
of the vocal cords during expiration and could represent an attempt to re-expand collapsed
parts of the lung.
Aust Vet J. 64: 142-144
Introduction
Although no studies have been undertaken to observe the
effects of Zxodes holocyclus on respiration, many authors
(Stuart 1894; Dodd 1921; Ross 1926; Ross 1935; Hamilton
1940; Roberts 1941; McCarthy 1958) concluded that death
was due to respiratory failure. Hamilton (1940), Roberts (1941)
and McCarthy (1958) stated that this failure arose peripherally
from paralysis of the muscles of respiration.
During previous investigations (Ilkiw et al 1987a) it was
observed that an early sign of the disease was a change in
respiratory pattern. The normal respiration was initially replaced by a “grunting” type, which progressed to laboured
slow breathing with feeble limb movements and grunts accompanying each breath.
The Forest Animal Hospital, 61 2 Warringah Rd, Forestville,
New South Wales 2087
142
As this type of respiration had not been noticed in dogs
with neuromuscular disorders (polyradiculoneuritis, myasthenia gravis and tiger snake envenomation), a detailed study
of the effects of Zxodes holocyclus on respiration in the dog
was carried out.
Materials and Methods
Fourteen healthy cross-bred dogs ranging from 11.0 to 23.5
kg were used in this study. One week prior to attachment of
the ticks the dogs were surgically prepared by implantation
of a catheter in the carotid artery to enable collection of
arterial blood.
The dogs were trained to lie quietly on a foam-rubber
padded table and to breathe normally through a facemask.
Expiratory vo!ume (VE), expiratory time (tE), expiratory minute volume (VE) and respiratory rate (f) were measured through
Australian Veterinary Journal, Vol. 64, No. 5, May, 1987