Measuring pain-perception and behavior of laminitic horses after
treatment (with addition of intramuscular Botox®).
Master research by Drs. A.A.H. Lamers.
Supervisors: Dr. J.H. van der Kolk, Dr. I.D. Wijnberg, Dr. W. Back.
From: Department of Equine Sciences, Utrecht University.
Date: July 2013.
Abstract
Objective: Laminitis in the horse causes failure of the distal phalanx to maintain its
attachment to the lamellae of the inner hoof wall. Also the constant traction of the
deep digital flexor tendon on the distal phalanx can cause the distal phalanx bone to
rotate. These changes cause unrelenting pain and a characteristic lameness (Pollit
2004) The aim of this study was to investigate whether treating acute laminitis
following a treatment protocol, in addition of injecting Clostridium botulinum toxin
type A (Botox®) in the muscle belly of the deep digital flexor muscle, will lead to a
substantial pain relief and thus an increase in comfort of the horse, resulting in a
decrease in free-cortisol concentrations in saliva, and a lower result in compositepain-score after treatment.
Method: Literature research has led to a behavior protocol to measure painperception and behavior in the horse suffering from laminitis. Also a protocol for
cortisol determination was developed to indicate the amount of stress the horse
experiences. Two groups of horses was included in the study. A control group of ten
healthy warmblood horses was used to determine base-cortisol values in plasma
(total-cortisol concentration) and saliva (free-cortisol concentration). In the treatment
group, two horses suffering from acute laminitis were included. They were treated for
laminitis following a protocol, with addition of intramuscular bilateral Botox®. At
specific days post treatment (d0, d3, d7, d14) cortisol was measured in plasma and
saliva, and they were scored following a composite-pain-score.
Results: In contrast to earlier findings (Van der Kolk et al. 2001), we were unable to
find normally distributed values of salivary cortisol in healthy horses. Cortisolconcentrations in plasma on the other hand, were indeed normally distributed. Patient
I showed a nice decrease of plasma and salivary cortisol at day 3 and day 7. However,
at day 14 there was an extreme rise in both plasma and salivary cortisol. Also the
pain-score showed a decrease in the first days, and rising at day 14. Patient II showed
an increase of both plasma and salivary cortisol at day 3, however, at day 7 and 14 it
decreased back to normal. The pain-score on the other hand, showed higher scores at
day 14.
Conclusion: Both patients showed a decrease in cortisol-concentration after
treatment. Unfortunately, the group was small (n=2) and there were underlying
illnesses present in these horses that very likely might have influenced our results.
Also the pain scores were influenced in this way. To reveal the value of cortisoldetermination in monitoring laminitic patients, more research has to be done in which
more patients are involved and circumstances can be more standardized.
A.A.H. Lamers
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General introduction
Laminitis in the horse causes failure of the distal phalanx to maintain its attachment to
the lamellae of the inner hoof wall. Also the constant traction of the deep digital
flexor tendon on the distal phalanx can cause the distal phalanx bone to rotate. These
changes cause unrelenting pain and a characteristic lameness. This condition can be
reached via changes in various mechanisms; including vascular, enzymatic,
inflammatory, hormonal, mechanical, or a combination of these factors. Therefore,
therapeutic intervention has to intervene in all of these mechanisms. Nowadays, the
use of a multimodal therapy including anti-inflammatory medication, multi-modal
pain management and farriery seems to be the best option for treatment (Bailey et al.
2004; Moore 2008; Morrison 2004; O'Grady 2010; Orsini et al. 2009). However, it is
suggested that still 50% of all acute laminitic patients eventually suffer from
foundering or sinking of the distal phalanx thereby becoming chronic (Pollit and
Collins 2011). Once the distal phalanx has displaced within its hoof capsule, the
prognosis for survival of the laminitic patient strongly decreases (Cripps and Eustace
1999).
Botox®
In laminitic horses the constant traction of the deep digital flexor tendon (DDFT) on
the distal phalanx can cause the distal phalanx bone to rotate. (Pollit, 2004) Tenotomy
of the DDFT relieves the pulling of the deep digital flexor muscle on the distal
phalanx, preventing the rotation of the pedal bone within the hoof wall. (Orsini et al.
2009, Eastman et al. 1999, Morrison 2011) This surgery can be a live-saving
treatment of acute laminitis and gives immediate and often substantial pain relief.
(Hunt et al. 1991, Orsini et al. 2009) Nevertheless, transection of the DDFT has been
reported with variable success rates in the previously published data. As in every
surgery there are risks that come with this procedure. Tenotomy can lead to limited
athletic performance, persistent lameness, and the survival rate of affected horses may
not be altered. (Morrison 2011, Eastman et al. 1999, Hunt et al. 1991)
Paralyzing the deep digital flexor muscle by injecting Botox® into the muscle belly
would obviate the need for the surgery (and the surgical risks would be removed). In
Carter’s research (2009), seven horses with varying degrees of laminitis were
evaluated. Each horse received botulinum toxin type A injected into the belly of the
deep digital flexor muscle. In all cases there was radiologic stabilization of pedal
displacement from the dorsal hoof wall. Also the degree of lameness improved
significantly after treatment. The usage of Botox® in horses with locomotion
problems (stringhalt) has been applied without signs of intoxication at the department
of Equine Sciences, University Utrecht (Wijnberg, I, 2008). Because the lack of
therapies to treat laminitis and the good results of using Botox® in the horse in
reducing muscle tone (Wijnberg, I. 2008), we hypothesize that the use of Botox® in
case of acute laminitis will be a successful supportive therapy.
Stress and cortisol
Stress is a state that results in an increased activity of the Hypothalamo-PituitaryAdrenal Axis (HPA-axis), which results in increased cortisol production. Cortisol is
A.A.H. Lamers
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2
transported in the blood primarily in association with binding proteins called
corticosteroid-binding globuline (CBG). (Alexander and Irvine, 1998) Stress affects
the adrenal axis, lowering the binding capacity of CBG and raising bioactive “free”
cortisol concentrations.
Measurement of only total plasma cortisol concentration may not accurately reflect
changes in the HPA-axis. (Alexander and Irvine, 1998) Thus, preference should be
given to measurement of free cortisol, which can be achieved via assessment of
cortisol-concentration in saliva. Only the unbound cortisol can cross into saliva. (Van
der Kolk et al. 2001) (Reijerkerk et al. 2009)
Pain and behavior
As pain is a complex multi-dimensional experience consisting of behavioral,
physiological and emotional aspects, there is no single parameter that specifically
indicates the presence of pain. Therefore pain assessment can be challenging and must
rely on an appreciation of normal animal physiology and behavior (van Loon et al.
2010, Lerche et al. 2009). Various scoring systems employing either behavioral
characteristics only or both behavioral and physiologic parameters have been
developed to monitor pain in horses. (Obel. 1948, Dutton et al. 2009, Driessen et al.
2010) Physiological parameters used alone to identify and grade painful states in
animals have been shown to be inadequate (Bussières 2008). Combined interactive
(dynamic: as the horse moves or responds to a stimulus) and observational (Static:
behaviors the animal displays undisturbed) multifactorial pain behavior rating scales,
used in combination with physiological parameters, may be more sensitive in
identifying changes due to pain in animals. (Dutton et al. 2009)
Previous studies show a variety of parameters that indicate laminitic pain. Such as
resistance to weight bearing on the hoof (shifting back and forth between hooves),
increased heart rate variability, spending more time at the back of the box, reluctance
to move, frequently lying down, decreased appetite.
Study objective
The aim of this study is to test the hypothesis:
Treating acute laminitis following a treatment protocol, in addition of injecting
Clostridium botulinum toxin type A (Botox®) in the muscle belly of the deep digital
flexor muscle will lead to a substantial pain relief and thus an increase in comfort of
the horse, resulting in a decrease in free- cortisol concentrations in saliva, and a lower
result in composite-pain-score after treatment.
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Materials and methods
Literature research has led to a behavior protocol to measure pain and welfare in the
horse suffering from laminitis. Also a protocol for cortisol determination was
developed to indicate the amount of stress the horse experiences.
Animals
Control group:
Ten healthy Dutch Warmblood mares were used to determine base-morning-cortisol
values. All of them are long-term residents at the department of equine sciences,
Utrecht University, kept under similar environmental conditions and accustomed to
frequent handling.
Treatment group:
To be included in this prospective study horses had to suffer from acute laminitis
defined by no rotation of the distal phalanx, with the possibility to be treated within
48 to 72 hours after the onset of the first symptoms. Their lameness from laminitis
had to be scored as Obel grade 2 or 3 (Appendix 1) with no radiographical changes of
laminitis yet. A standardized laminitis treatment protocol was initiated for every case
and consisted of meloxicam (Metacam®) 1ml/28 kg bodyweight on the first day and
phenylbutazon (Pro-Dynam®) 4,4 mg-kg bodyweight twice daily on the second, third,
fourth and fifth day followed by 2,2 mg/kg twice daily for analgesia and antiinflammation, carbasalate calcium (Ascal®) 10 mg/kg bodyweight on the first day
followed by 5 mg/kg bodyweight a day for anticoagulation and acepromazine
(Tranquigel®) 0,3-0,6 ml/100kg bodyweight four times a day for vasodilatation.
Shoes were removed, hooves were cooled and movement was limited by strict stall
rest. Food was limited to good quality hay.
In addition of this protocol, the muscle belly of the deep digital flexor muscle was
injected at five different locations with Botox® using ultrasound guidance (Hardeman
et al. 2012, 2013). Every 100 IU of Botox® was diluted with 2,5 ml NaCl 0,9%. First,
he caudal part of both forelegs was shaved and cleaned. Second, the distance between
the top of the olecranon and the os carpi acessorium was measured. Based upon an
earlier study on cadaveric forelimbs, the distance was used to determine five points in
the widest part of the muscle belly. Afterwards the leg was disinfected using alcohol.
The needle was inserted in the groove between the flexor carpi ulnaris muscle and the
flexor digitalis superficialis muscle, injecting five times 1 ml diluted Botox® per leg.
To distribute the Botox® evenly among the deep digital flexor muscle, one injection
was placed in the superficial part, two injections in the middle part and two in the
deep part of the deep digital flexor (Figure 2). Injections were guided by ultrasound to
guarantee the correct position of the injection needle. Solution was injected through
an EMG Myoject® Needle Electrode (length 75 mm, diameter 0.71 mm, recording
area 0.89 mm2 ), with a monopolar needle (length 75 mm, diameter 0.46 mm,
recording area 0.34 mm2).
Clinical monitoring for the study was performed at day 0, day 3, day 7 and day 14.
Cortisol determination
To measure free cortisol concentrations, blood- and saliva samples were taken at days
0, 3, 7 and 14 after treatment between 1100 hr and 1300 hr. Blood samples were taken
from the jugular vein and collected in blood collection tubes with EDTH and heparin.
Saliva samples were taken using cotton-balls.
A.A.H. Lamers
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The blood samples were centrifuged at 6000g for 5 minutes. The supernatant plasma
and the saliva was put into separate Eppendorf tubes and saved in the freezer at -20
°C. The cortisol was measured in a laboratory after validation using a Luminescent
immunoassay test. (LIA; Siemens Medical Solutions Diagnostics) validated for use in
horses (Van der Kolk et al. 1995).
Behavior protocol
Various scoring systems employing either behavioral characteristics only or both
behavioral and physiologic parameters have been developed to monitor pain in horses.
(Obel. 1948, Morton et al. 2005, Dutton et al. 2009, Driessen et al. 2010) Obel (1948)
was among the first to describe a grading system for lameness in horses affected by
laminitis. Dutton et al. (2009) recently applied a modified composite multifactorial
pain scoring system that includes components of the Obel Grading System and the
Glasgow composite pain scale in a horse suffering from severe persistent foot pain.
We have made a combination of various scoring systems, which will make the scoring
even more accurate(Appendix 1).
Results
Control group:
Ten healthy Dutch Warmblood mares were used to determine base-morning-cortisol
values in bloodplasma and saliva. The outcomes were variable, with a mean of 87,5 ±
6,47087 in plasma and a mean of 11,8010 ± 3,75243 in saliva.
The outcomes were tested for normality, using a shapiro-wilk-test. This, because we
are dealing with a group of less than 50 animals. Data are normally distributed, if
significance is >0,05. In contrast to earlier findings (refs, vd kolk et al.), we were
unable to find normally distributed values of salivary cortisol (significance: 0,001).
Cortisol-concentrations in plasma, on the other and, were indeed normally distributed
(significance: 0,345). (Fig 1.)
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Fig. I: Morning cortisol levels of ten healthy horses.
Plasma:
Saliva:
Treatment group:
Patiënt I
Patiënt I was an eight-year-old Irish Cob gelding admitted to the hospital with colic.
Colic surgery resolved a right dorsal colon constipation. Six days after the colic
surgery, the horse started to show laminitis Obel Grade 3 with no radiologic
displacement of the distal phalanx (D0). At that time the horse was treated with
Botox® using ultrasound guidance in both front limbs. At D3 and D7 the horse had
dropped to an Obel Grade 2 lameness, still showing no radiological distal phalangeal
rotation and/or displacement. At D14, the lameness of the horse was still scored Obel
grade 2. However, his general condition deteriorated showing a high pulse and central
edema. Two days later he died of an unknown cause, while at pathological
examination not any signs of laminitis could be detected.
Patiënt I initially showed a nice decrease of plasma and salivary cortisol at day 3 and
day 7. However, at day 14 there was an extreme rise in both plasma and salivary
cortisol. (Fig 2) Also the pain-score showed a decrease in the first days, and rising at
day 14. (Fig 3)
A.A.H. Lamers
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Fig. 2: Patient I, Plasma- and salivary cortisol.
Fig. 3: Patient I, Composite-pain-score.
Composite-pain-score (adapted from van Loon
et al. 2010 and Bussières et al. 2008)
day 0 day 3 day 7
day 14
Score
5
4
1
4
Modified composite-pain-score
(Dutton et al. 2009)
Day 0 Day 3 Day 7
Score
3
6
2,5
(MCPS)
Day 14
3
Patiënt II
Horse II was an twelve-year-old Royal Dutch Sport horse admitted with the complaint
of poor performance. After 13 days after admittance to the clinic, the horse developed
signs of laminitis, an Obel grade 2 lameness and a strong digital pulse on both front
feet, but no radiological displacement of the distal phalanges. At that time (D0), the
horse was treated with Botox®. At D3 the digital pulse was reduced to normal levels
and its lameness was rated Obel grade 1. At D7 and 14, the digital pulse on both front
feet was only minimal and its lameness was still Obel grade 1, again without any
radiological changes in the distal phalanges. However, 35 days after treatment its
condition deteriorated fast and showing increased lameness from laminitis as an Obel
grade 3. Radiological findings were rotation and sinking of the distal phalanges. At
that time, the owner decided to have the horse euthanized.
Patiënt II showed an increase of both plasma and salivary cortisol at day 3, however,
at day 7 and 14 it decreased back to normal. The pain-score on the other hand, showed
higher scores at day 14.
A.A.H. Lamers
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Fig. 3: Patient II, plasma- and salivary cortisol.
Fig. 4: Patient II, composite-pain-score.
Composite-pain-score (adapted from van Loon
et al. 2010 and Bussières et al. 2008)
day 0 day 3 day 7
day 14
Score
0
1
0
4
Modified composite-pain-score
(Dutton et al. 2009)
Day 0 Day 3 Day 7
Score
3
2
2
A.A.H. Lamers
(MCPS)
Day 14
3
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Discussion
The aim of this study was to investigate whether treating acute laminitis by injecting
Clostridium botulinum toxin type A (Botox®) in the muscle belly of the deep digital
flexor muscle will lead to a substantial pain relief and thus an increase in comfort and
welfare of the horse suffering from laminitis.
Unfortunately, the outcome of the base-values of free cortisol in saliva was not
normally distributed, which makes it difficult to compare the results of the patients
with those of the control group. This can be due to the fact that it was a small group of
horses (n=10). Also it can refer to the circadian rhythm of cortisol. Horses have a
circadian rhythm in plasma glucocorticoid concentrations, with a peak between 6.00
and 9.00 hr and a trough between 19.00 and 23.00 hr. (Stull and Rodiek 1988) (Irvine
and Alexander 1994). We had to take samples in quite a broad marge, between 1100
hr and 1300 hr due to practical problems in reaching the patients. It would have been
more accurate if we could take the samples at exact the same time each testing day.
Also, it has been described that this rhythm can easily be disturbed or changed by e.g.
placing horses in a novel environment. (Irvine and Alexander 1994) Horses suffering
from acute laminitis are usually not hospitalized, unless they are already at a clinic
and laminitis occurs as a complication of another illness. This was the case in our
patients. Those underlying illnesses might have influenced our results and might very
well have resulted in the experienced final, fatal complications in both patients.
Patient I initially responded well to treatment. Both composite-pain-score and cortisol
levels dropped nicely. However, at the time of D14, his general condition
deteriorated. Most likely, this came with a rise in pain- and stress levels, which
resulted in the extreme rise in both cortisol-concentration and composite-pain-score at
day 14.
Patient II initially responded well to treatment but still that could not prevent its fatal
laminitis from occuring. To date, it is not known what triggered this laminitis. The
second, fatal onset of laminitis started 35 days after the initial treatment, although
botox is thought to maintain its action for three months. (Wijnberg et al. 2009)
To reveal the value of cortisol-determination in monitoring laminitic patients, more
research has to be done in which more patients are involved and circumstances can be
more standardized.
A.A.H. Lamers
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Appendix 1
Composite pain score (adapted from van Loon et al. 2010 and Bussières et al. 2008)
Patient:
Date:
Time:
Observer:
Interactive
behavior
Score
Pays attention to people
Exaggerated response to auditory stimulus
Excessive-to-aggressive response to auditory stimulus
Stupor, prostration, no response to auditory stimulus
0
1
2
3
Bright, lowered head and ears, no reluctance to move
Bright and alert, occasional head movements, no
reluctance to move
Restlessness, pricked up ears, abnormal facial
expressions, dilated pupils
Reluctance to move, stands or lies down at the back of
the box
0
1
Appearance
2
3
Appetite
Eats hay readily
0
Hesitates to eat hay
1
Shows little interest in hay, eats very little or takes hay 2
in mouth but does not chew or swallow
Neither shows interest in nor eats hay
3
Posture
Quietly standing or walking
Occasional weight shift or slight muscle tremors
Frequent weight shift, frontlegs are placed forward
Lies down
0
1
2
3
Sweating
No obvious signs of sweat
0
Damp to the touch
1
Wet to the touch, beads of sweat are apparent over the 2
horse’s body
Excessive sweating, beads of water running off the 3
animal
Respiratory rate
8-13 breaths/min
14-16 breaths/min
17-18 breaths/min
>18 breaths/min
0
1
2
3
Now the observer can gently enter the stable.
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2
Heart rate
24-44 beats/min
45-52 beats/min
53-60 beats/min
>60 beats/min
Score
0
1
2
3
Rectal temperature
36.9-38.5
36.4-36.8 or 38.6-39.0
35.9-36.3 or 39.1-39.5
35.4-35.8 or 39.6-40.0
Maximum possible score: 24
0
1
2
3
Modified composite pain score (MCPS) (Dutton et al. 2009)
Dynamic score:  1
Modified
Obel
Grading System
2
3
Frequent shifting of weight between the feet with no
discernible lameness at the walk.
Does not resist having a foreleg lifted, is not reluctant to
walk, but does show lameness at the walk.
Resists having a foreleg lifted and is reluctant to walk.
4
Walks only if forced.
Static
score:  1
Modified
from  2
Glasgow
3
composite scale
4
5
6
7
8
9
No pain or distress: normal behavior.
Mild pain: irritable, restless, decreased appetite.
Mild pain: 2 plus resists handling.
Mild-moderate pain: 3 plus standing in back of stall or with
back to stall door.
Moderate pain: 4 plus camped-out legs, increased digital
pulses.
Moderate-severe pain: 5 plus frequent recumbency, HR >44
beats/min, and/or RR >24 breaths/min.
Moderate-severe pain: 6 plus sweating, muscle
fasciculation, head-tossing.
Severe pain: 7 plus unwilling to move.
Severe-extreme pain: 8 plus not weight bearing when
standing.
Extreme pain: 9 or entirely recumbent, bordering on agonal.

10
Maximum possible score: 14
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3