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V. Molony and J. E. Kent
measurements
Assessment of acute pain in farm animals using behavioral and physiological
1997, 75:266-272.J ANIM SCI
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266
1
Presented at a symposium titled “Effects of Stress in Farm
Animals” at the ASAS 87th Annu. Mtg., Orlando, FL, July 26, 1995.
2
The authors wish to thank the Agricultural & Food Research
Council, the Ministry of Agriculture Fisheries & Food, the Scottish
Office Agriculture & Fisheries Department, the Meat & Livestock
Commission and the Moredun Foundation for their support. We are
also grateful for statistical advice from staff of the Scottish
Agricultural Statistics Services, Edinburgh.
Received August 25, 1995.
Accepted September 10, 1996.
Assessment of Acute Pain in Farm Animals Using Behavioral
and Physiological Measurements
1,2
V. Molony and J. E. Kent
Department of Preclinical Veterinary Sciences, Royal (Dick) School of Veterinary Studies,
University of Edinburgh, Edinburgh EH9 1QH, Scotland
ABSTRACT: In this paper various aspects of
animal pain and methods for its assessment are
considered. The responses of lambs and calves to
castration and of lambs to tail docking are used to
illustrate quantitative approaches to the recognition
and assessment of acute pain in farm animals. The
validation of physiological and behavioral measure-
ments for assessment of pain is examined by relating
measurements made from young lambs, after a range
of treatments, to an independent ranking of the order
of severity of the treatments.
Key Words: Pain, Hydrocortisone, Behavior, Castration, Docking, Discriminant Analysis
J. Anim. Sci. 1997. 75:266–272
Introduction
The development of methods of recognition and
assessment of animal pain has been delayed by the
unwillingness of some people to accept that animals
are capable of experiencing or suffering pain when
subject to injury, disease, or other noxious events.
This may be due to expediency or to confusion of
animal with human pain. For this paper it is assumed
that animal pain generally serves the same purposes
as human pain and that the experiences are similar,
but that animal and human pain are not the same
(Molony, 1986, 1992).
The following working definition of animal pain is
used for this paper: animal pain is an aversive sensory
and emotional experience representing an awareness
by the animal of damage or threat to the integrity of
its tissues; it changes the animal’s physiology and
behavior to reduce or avoid damage, to reduce the
likelihood of recurrence and to promote recovery;
unnecessary pain occurs when the intensity or dura-
tion of the experience is inappropriate for the damage
sustained or when the physiological and behavioral
responses to it are unsuccessful at alleviating it.
Although physiological and behavioral changes are
used here to define the presence and intensity of the
experience, more studies are required to determine
which changes to measure and how this can be
achieved so that they can be applied to individual
animals under clinical (field) conditions.
For unequivocal examples of animals in pain that
might be ethically acceptable models for investigation,
we turned to castration and tail docking of lambs and
castration of calves. These practices are carried out
with two main justifications: they improve the overall
welfare of the animal, and the economic benefits
outweigh the welfare costs. It is not intended to debate
this here, but it seems reasonable that those carrying
out such practices should be aware of how much pain
they cause, and that they should support efforts to
find the most humane ways of carrying them out.
The studies described in this paper were justified on
two grounds: first, as part of the search for more
humane methods for the procedures; and second,
because the lambs or calves would normally be
subjected to the procedure as part of an accepted
husbandry system. This helped to obtain the permis-
sion of the licensing authorities in the UK (Home
Office).
The studies are based on those used for the general
assessment of pain (Chapman et al. 1985; Sandford et
al., 1989), pain in young children (McGrath, 1987),
and for assessment of pain produced in experimental
animals by subcutaneous formaldehyde (Dubuisson
and Dennis, 1977; Coderre et al., 1993; Abbott et al.,
1995) or by sciatic ligatures (Bennett and Xie, 1988;
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ASSESSMENT OF ACUTE PAIN IN FARM ANIMALS
267
Attal et al., 1989; Attal et al., 1990; Kupers et al.,
1992).
Following the introduction of some principles for
assessment of pain, evidence for acute pain from
castration and tail docking will be discussed, and an
attempt to validate some indices for assessment will
be described.
Principles for Assessment of Animal Pain
Because direct measurement of subjective ex-
periences is not possible, assessment of animal pain is
of necessity a value judgment relying on physiological
and behavioral indices to provide indirect evidence of
this particular mental state. Several different indices
ought normally to be used and their evaluation should
be improved by training and experience. Those in the
best position to make judgments will know the species,
breed, and individual animal well; they include
veterinary surgeons, farmers, and stockmen and
stockwomen. To give animals the benefit of any doubt,
where there is a choice, judgments should overesti-
mate the intensity of pain to avoid missing animals in
pain at the cost of treating some that are not.
Humans have a highly developed capacity for
accurately appreciating the feelings of at least some
other humans; this capacity may be misused, however,
by applying it to humans from very different cultural
backgrounds, to animals that have different cerebral
capacities, and even to inanimate objects such as soft
toys. Observation of an event that would be noxious if
applied to the observer may thus illicit unwarranted
empathetic feelings and emotional responses, and
observers should make allowance for this in their
assessment of animal pain.
Types of Animal Pain
Acute and chronic pain occur over different time
courses: acute pain does not outlast the healing
process, whereas chronic pain persists beyond the
expected healing time for an injury. Acute pain is
generally accompanied by autonomic changes and
responds to analgesic treatment. Acute recurrent pain
is a term that can be used to describe prolonged pain,
such as cancer pain, which has a definable cause and
consists of repeated attacks of acute pain. Chronic
pain may have no obvious cause or temporal onset
(American Pain Society, 1987).
Somatic and visceral pain originate in different
parts of the body and have other notable differences
(e.g., somatic pain is generally well localized, whereas
visceral pain is poorly localized and may be referred to
distant parts of the body).
Pain originating within the peripheral or central
nervous system is often chronic and may not be
dependent on activity from nociceptors; it seems to be
produced by damage to the mechanisms underlying
the pain process and its control.
Types of Pain Response
Several types of responses can be recognized: 1)
those that modify the animal’s behavior by learning
and so enable the animal to avoid recurrence of the
experience; 2) those, often automatic, that protect
parts or the whole animal (e.g., withdrawal reflexes);
3) those that minimize pain and assist healing (e.g.,
lying or standing still); and 4) those that are designed
to elicit help or to stop another animal (including
humans) from inflicting more pain (e.g., communica-
tion by vocalization, posture, or other means such as
smell).
Physiological and Behavioral Evidence for Acute
Pain After Castration and(or) Tail Docking
Activity in Afferent Nerves.
It has been shown that
castration and tail docking of lambs with rubber rings
produces significant increases in the afferent activity
from nociceptors in the testes and tail (Cottrell and
Molony, 1995; Graham, personal communication
1996). Increased activity of nociceptors with similar
properties can be recorded directly from the nerves of
conscious humans who report the stimulation as
painful (Rice and Casale, 1994). The time course of
the increase in nociceptor activity after these proce-
dures can be related to increases in plasma cortisol
and increases in abnormal behavior.
Activity of the Sympathetic Nervous System. There
are several ways of measuring the activity of the
sympathetic nervous system, including changes in
heart rate, pupillary diameter, skin resistance, and
peripheral blood flow. Because the system generally
works as an integrated whole, several of these changes
may occur in parallel. The state of the system can
most easily be assessed by monitoring the heart rate
from an electrocardiogram or by serial measurements
of plasma catecholamines. Changes in heart rates of a
limited number of animals subjected to castration
have been measured (Kent et al., unpublished obser-
vations), and although changes consistent with
predicted pain were detected, there were many inter-
fering variables such as eating, exercise, and extrane-
ous noises. It would therefore be difficult to use such
changes in heart rate as a practical index for
assessment of pain.
Activity of the Hypothalamo-Pituitary-Adrenal Axis.
This is most easily measured from levels of cor-
ticosteroid hormones in plasma or saliva. A series of
measurements must be made both before and after the
treatment to accommodate the characteristics of
release and elimination of the hormones and to
determine the changes produced. Changes in plasma
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MOLONY AND KENT
268
cortisol concentrations closely follow the time course of
changes in posture and activity after castration and
tail docking (Kent et al., 1993). There are, however,
interfering variables that can limit the use of such
measurements for assessment of pain, including in-
dividual variation, diurnal changes, and the wide
variety of stressors that activate the hypothalamic-
pituitary-adrenal system.
Changes in Posture. Postural changes can be volun-
tary or involuntary. Involuntary spinal and brainstem
reflexes can be initiated by activity from nociceptors,
some of which may cause hyper-reflexia, including
increased muscle tone; an example of this may be seen
after castration of lambs with rubber rings as full
extension of the hind limbs (Molony et al., 1993b). A
voluntary change in posture after castration may be
the adoption of an immobile stance (statue standing)
to avoid or reduce stimulation of hyperalgesic tissues.
Under experimental conditions, the changes in
posture after different methods of castration or tail
docking can be compared with changes exhibited by
animals subjected to sham treatments. Many different
postures are available for use as indices, including
various forms of lying and standing categorized
according to the positions of the limbs and head. These
postures have been divided somewhat arbitrarily for
lambs into 1) normal lying, ventral (sternal) with the
head down ( V
1
), with the head up (V
2
), both
occurring frequently in sham-treated lambs; 2) abnor-
mal lying, ventral with partial extension of one leg
( V
3
) or full extension of one or more legs (V
4
), and
lateral lying with a shoulder down and the head up
( L
1
) or down (L
2
), none of which occurred in control
lambs under the environmental conditions for these
experiments experienced in Scotland; 3) standing
postures including normal standing/walking (S
1
),
abnormal standing/walking with just detectable
ataxia, swaying, or abnormal stance ( S
2
), grossly
abnormal standing/walking with stilted gait walking
on knees or walking backward (S
3
), and immobile or
statue standing ( SS) (Molony et al., 1993b, 1995).
The time spent by lambs in these postures after
castration and(or) tail docking when compared with
that spent by control lambs indicates how much the
treatments changed behavior. The prevalence of par-
ticular postures or activities after treatments of
different severities helps determine any weighting
given to them as indices.
Changes in Locomotor Activity. In addition to
changes in posture, castration and tail docking
produce increases in locomotor activity, including
restlessness, kicking, stamping, rolling, jumping, eas-
ing quarters, licking/biting at the site of damage, and
tail wagging; the incidence of these behaviors can
increase until all of the animal’s time is spent in
“abnormal” active behavior (Molony et al., 1993b).
Although some of these active responses seem to have
no beneficial effects, they may be generally described
as attempts to escape and may represent specific pain
behavior. They are usually replaced by abnormal
postures when the animal alters its strategy from
active to passive attempts at avoidance.
Fatigue also contributes, because prolonged active
behavior uses up reserves of energy (changes plasma
glucose and FFA), produces heat (increases body
temperature), and causes metabolic and electrolyte
changes including acidosis and dehydration, all of
which can be measured as physiological changes but
none of which has been shown to be a specific index for
pain.
Changes in Evoked Behavior. Intense noxious stimu-
lation by castration and tail docking leads, in some
lambs, to periods of inert lateral lying (Molony et al.,
1993b) during which it can be difficult to elicit any
evidence of conscious awareness. Some ewes paw
vigorously at their lambs when they see them lying
immobile in this lateral posture; this seems to be a
way of evoking activity to help alleviate the ewe’s
concern for the “state” of its offspring. It illustrates a
common approach to assessment of the “state” of a
lamb by both ewe and shepherd.
Part of any assessment of pain should include the
animal’s response to standard stimuli, the commonest
being its response to the approaching shepherd or
sheepdog. Systematic experimental use of evoked
responses has been by means of tests such as the open
field test (Fell and Shutt, 1989).
Reduction of Physiological and Behavioral Changes by
Local Anesthetic Treatment.
Local anaesthetic treat-
ment can reduce or eliminate both physiological and
behavioral changes produced by castration and tail
docking by blocking transmission of neural activity
from the affected tissues, thus confirming the
peripheral nociceptive basis of this acute pain (Wood
et al., 1991).
Reduction of Physiological and Behavioral Changes by
Analgesic Treatment.
Although some analgesia has
been achieved in sheep with opioids, a
2
agonists and
nonsteroidal anti-inflammatory drugs (NSAID) (No-
lan et al., 1987; Waterman et al., 1991; Ley et al.,
1991; Welsh et al., 1992), no systematic dose-related
reductions of the physiological and behavioral changes
produced by castration and tail docking have been
achieved. Of the analgesics tried, xylazine (an a
2
agonist) reduced both physiological and behavioral
responses to tail docking (Molony et al., 1993a), and
diclofenac, a NSAID, was effective against the pain
produced by burdizzo castration but not against that
produced by rubber ring castration or tail docking
(unpublished observations). The opioids morphine
and etorphine, however, when administered intrathe-
cally, had no effect on responses to castration and tail
docking (Wood, 1991; Molony and Wood, 1992). More
studies are required to demonstrate a clear dose-
response relationship between indices of pain from
castration and tail docking and increasingly effective
doses of analgesics. However, it seems that the
visceral (testicular) pain produced by rubber ring
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ASSESSMENT OF ACUTE PAIN IN FARM ANIMALS
269
Figure 1. Responses of groups of 5- to 6-d-old Dorset crossbred lambs (n = 7) to the following treatments of
decreasing severity: castration and tail docking (C+TD); bilateral castration (C*2); unilateral castration (C*1); short
scrotum castration (C*0); tail docking (TD); short scrotum castration + local anesthesia (C*0+LA); or handled controls
(H). (a) The mean (± SD) times spent lying during the 180 min after treatment. (b) The mean (± SD) times spent lying
abnormally (V
4
) during the 180 min after treatment. (c) The mean incidences (± SD) of restlessness + roll/jumping +
foot stamp/kicking + easing quarters (REQ) during the 180 min after treatment. (d) The mean (± SD) peak cortisol
concentrations (nmol/L) reached during the 180 min after treatment. The median value for each group is indicated by
the full-width horizontal line. Mean values for treatment groups labelled with the same letter are not significantly
different (P > .05).
castration may be resistant to alleviation by com-
monly used analgesics, and indices for measuring this
pain cannot be validated if they are also required to
assess the effectiveness of the analgesic.
Validation of Indices and Elimination
of Redundant Indices
For clinical assessment of pain it is necessary to
determine the validity and sensitivity of each index
and to eliminate as many redundant indices as
possible. This has been attempted using indices alone
or in combinations, to assign animals to a series of
groups ranked in order of decreasing severity of
treatment based on alternative independent indices.
An abstract with some results is included to illustrate
the approach.
Methods
Forty-nine Dorset crossbred lambs weighing 3 to 6
kg were penned (3.6 m × 1.5 m) with their dams and
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MOLONY AND KENT
270
Table 1. Discriminant analysis with cross-validation using posture V
4
a
and the REQ
b
score
c
a
V
4
= ventral lying with full extension of the hindlegs.
b
REQ = summation of restlessness, roll/jumping, foot stamp/kicking, and easing quarters.
c
Lambs in different treatment groups (Actual) are assigned to a group according to the V
4
/REQ values obtained after treatment.
d
No. = 49.
e
No. correct = 31.
f
Proportion correct = .633.
Assigned
group
Actual group
C+TD C*2 C*1 C*0 TD C*OLA H
C+TD 5 100000
C*2 1 4 10000
C*1 1 1 4 0000
C*0 0 1 2 4 100
TD 0003420
C*OLA 0000130
H 0000127
Total no.
d
7777777
No. correct
e
5444437
Proportion
f
.71 .57 .57 .57 .57 .43 1.00
siblings. Groups of seven lambs were treated at 5 or 6
d old. The treatments were ranked before the experi-
ment in decreasing order of severity according to the
amount of tissue involved and the established effec-
tiveness of local anesthetics, thus providing a rank
order of severity.
1. Bilateral castration and tail docking with rubber
rings ( C+TD).
2. Bilateral castration with a rubber ring (C*2).
3. Unilateral castration with a rubber ring (C*1).
4. Short scrotum castration with a rubber ring: the
testes were pushed up into the inguinal region and
the ring placed around the neck of the scrotum
( C*0).
5. Tail docking with a rubber ring ( TD).
6. Short scrotum castration with a rubber ring plus
.3 mL of local anesthetic (Bupivacaine .25%) into
the neck of the scrotum on each side just proximal
to the rubber ring (C*0+LA).
7. Handled controls ( H).
It was considered that the increments in severity
between treatments C*0, C*1, and C*2 were most
likely to be similar. Ranking of TD was uncertain
because different tissue and a different location were
involved.
Plasma cortisol concentrations were measured be-
fore ( −20 min and 0 min) and at intervals for 180 min
after treatment (nine samples). Postures (scanned at
2-min intervals) and active behaviors (continuous)
have been described above; they were recorded by
direct observation for 180 min as in previous studies
(Molony et al., 1993b). Statistical analysis was by
one-way analysis of variance; significant differences
between groups were established using Student’s t-
tables and the standard error of the difference. To
investigate the value of different indices alone and in
combination, cross-validated discriminant analysis
(Minitab v9) was carried out. This measured the
proportion of lambs that could be assigned to appropri-
ate (correct) treatment groups using the values
obtained for particular indices.
Results
Examples are presented of the relationships be-
tween the different indices investigated and the
intensity of pain as predicted from the order of
severity of the treatment.
Lying (total) during the 180 min after treatment
(Figure 1a) was not different in any of the treatment
groups ( P > .05). Abnormal ventral lying (V
4
)
separated the four most highly ranked groups from
the rest ( P < .05; Figure 1b), and the sum of the
scores over 180 min for restlessness, rolling, foot-
stamping/kicking and easing quarters (REQ) sepa-
rated the treatments from each other (P < .05) except
C*1 from C*0 (Figure 1c). Peak plasma cortisol
changes did not distinguish between either the three
most or three least highly ranked treatments but
distinguished a treatment of intermediate severity
(C*0) from both the least and most severe groups (P
< .01; Figure 1d).
To find the most economical combination of the
indices used, they were subjected to cross-validated
discriminant analysis. A combination of V
4
and REQ
gave one of the best results, placing 63% of the lambs
in their appropriate treatment groups (Table 1);
addition of the peak cortisol response reduced this to
59% (Table 2).
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ASSESSMENT OF ACUTE PAIN IN FARM ANIMALS
271
Table 2. Discriminant analysis with cross-validation using posture
V
4
a
, REQ
b
score, and peak plasma cortisol concentration
a
V
4
= ventral lying with full extension of the hindlegs.
b
REQ = summation of restlessness, roll/jumping, foot stamp/kicking, and easing quarters.
c
No. = 49.
d
No. correct = 29.
e
Proportion correct = .592.
Assigned
group
Actual group
C+TD C*2 C*1 C*0 TD C*OLA H
C+TD 4 100000
C*2 2 4 10000
C*1 0 2 5 1000
C*0 1 0 1 4 000
TD 0002420
C*OLA 0000221
H 0000136
Total no.
c
7777777
No. correct
d
4454426
Proportion
e
.57 .57 .71 .57 .57 .29 .86
Discussion
These results are consistent with the hypothesis of
Wood (1991) and Molony (1991) that plasma cortisol
can exhibit a ceiling effect, a maximal response being
obtained when only one testis (C*1) was involved.
Some behavioral indices also showed ceiling effects,
but for rubber ring castration and tail docking of
lambs of this breed and age, a more economical index
for assessment of acute pain was obtained by combin-
ing the time spent lying ventrally (V
4
) and the
incidence of the active behaviors (REQ). Weighting of
the values of V
4
and REQ according to their contribu-
tions to the discriminant analysis could help provide a
single measuring instrument similar to those used for
assessment of formalin-induced pain in rats (Coderre
et al., 1993; Abbott et al., 1995). Further analysis
should determine the requisite minimum measure-
ment time for these indices to obtain a similar level of
discrimination, and if less than about 20 min, this
approach may be of clinical use for assessment of this
type of pain in individual lambs.
Implications
Animal pain can be recognized and assessed using
physiological and behavioral indices but different
types of pain in different species should be considered
separately before generalizations are made about the
value of particular sets of indices for assessment.
Assessment is improved by using several indices, each
of which changes over different parts of the range of
intensities of pain. Multivariate analysis can help
determine the weighting of indices to obtain the most
robust and economical methods of assessment for each
type of pain in each species. If assessments with such
methods are shown to be consistent with those made
by suitably experienced veterinary surgeons, stock-
men, and stockwomen, it will help in appreciation of
the methods used by such experienced people, and in
standardizing the assessment of acute pain in farm
animals.
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