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S71
© 2004 Universities Federation for Animal Welfare
The Old School, Brewhouse Hill, Wheathampstead,
Hertfordshire AL4 8AN, UK
Animal Welfare 2004, 13: S71-75
ISSN 0962-7286
Assessing pain in animals putting research into practice
PA Flecknell* and JV Roughan
Comparative Biology Centre, Medical School, Framlington Place, University of Newcastle, Newcastle upon Tyne NE2 4HH, UK
*Contact for correspondence and requests for reprints
Abstract
Our ability to assess pain in animals in clinical situations is slowly developing, but remains very limited. In order to develop appropriate pain
scoring schemes, numerous practical problems need to be overcome. In addition, we need to appraise realistically our current poor
state of knowledge. Development of new scoring systems must be coupled with the increased education and training of those respon-
sible for pain management, so that both the assessment and the alleviation of pain are steadily improved.
Keywords:analgesia, animal, animal welfare, pain, pain assessment, pain scoring
Introduction
The last decade has seen growing concern over the issue of
pain and distress in animals. This concern has been reflected
in a steady increase in interest in pain assessment and pain
management amongst veterinary surgeons and others.
Despite this increased interest and concern, the manage-
ment of animal pain remains poor. For example the use of
post-operative pain relief in companion animals is low
(Dohoo & Dohoo 1996; Capner et al 1999; Lascelles et al
1999; Raekallio et al 2003). Even if analgesic use were to
increase, pain management is likely to remain poor because
we still have virtually no practically applicable means for
evaluating the degree of pain, and hence the effectiveness of
our analgesic therapy, in any species. Without a method of
assessing pain we cannot determine the efficacy of anal-
gesic therapy in individual animals, nor determine when
therapy can be discontinued.
In a recent editorial (Short 2003), the need to develop a
number of aspects of pain management was highlighted
(individual points edited for brevity):
Medications the need to develop more medications, for-
mulations and treatment modalities.
Pharmacokinetics the need for more information on the
pharmacokinetics of analgesics in animals of different
species.
Vital signs the diagnosis of painful conditions and the
effectiveness of treatment need to be correlated with pain
scoring as a vital sign, coupled with scientific evidence of
drug bioavailability.
Knowledge the biggest challenges ahead of us will be
in the education of all those involved in managing animal
pain.
Client relations an understanding of how veterinary
surgeons discuss the various issues with their clients.
If the results of animal pain research are to influence clini-
cal practice, we must raise awareness and improve the
knowledge of veterinary clinicians and others involved in
animal pain management through better education. It is also
essential that research projects provide these people with
the appropriate tools to assess animal pain. Without com-
mitment and the expertise to assess pain, all of the remaining
action points become irrelevant. It is therefore important to
examine what pain assessment tools we have, and how
many of these are both appropriately validated and suitable
for general use.
Pain assessment in farm animals
Behavioural and endocrine indicators of pain in lambs,
cattle and pigs have been established by a number of differ-
ent research groups (Noonan et al 1994; Lester et al 1996;
Mellor & Stafford 2000; Molony et al 2002). These have
been developed largely to aid in the evaluation of the wel-
fare benefits of modifying standard agricultural practices
such as tail docking, castration and dehorning. It has been
repeatedly demonstrated that the use of local anaesthetics,
either alone or in conjunction with modifications to the
techniques commonly used, can reduce pain-related behav-
iours in lambs and cattle. Regrettably, economic considera-
tions have limited the widespread application of the results
of these studies. Recently, the practical application of
improved methods of docking and castration has been
demonstrated (Kent et al in press), and pain scored in a
field situation. The improved techniques increased the
time taken for castration and tail docking, and required the
purchase of an additional piece of equipment. It seems likely
that widespread application of the improved methodology
will require that these economic issues be addressed.
Since additional interventions, such as the administration of
additional analgesics, are rarely contemplated following
Universities Federation for Animal Welfare Science in the Service of Animal Welfare
S72 Flecknell and Roughan
these husbandry procedures, there has been less of a need to
develop a robust pain assessment system for general use on
farms. It is worth noting, however, that in the study quoted
above (Kent et al in press) shepherds were able to use
Visual Analogue Scoring (VAS) to correctly identify lambs
experiencing less pain as a result of improved techniques. In
some circumstances, identification of pain would lead to a
modification of clinical practice, for example after
Caesarean section in cattle. Although a high percentage
(68%) of specialist cattle veterinarians administer anal-
gesics after Caesarean section, attempts to develop practical
pain scoring schemes have not proven successful (Watts
2001). This is largely because of the very considerable dif-
ficulties entailed in developing such schemes, and this is
discussed further below. Despite these difficulties, it is
encouraging to note that several pharmaceutical companies
are now actively marketing NSAIDs (non-steroidal anti-
inflammatory drugs) for use in presumed painful conditions
in farm animals.
Pain assessment in companion animals
Two well-documented schemes for pain assessment in dogs
have been developed (Firth & Haldane 1999; Holton et al
2001). In addition, numerous studies using pain scoring sys-
tems based on Visual Analogue Scoring, Numerical Rating
Systems, or Simple Descriptive Scores, or using a mixture
of all three approaches have been published (Brodbelt et al
1997; Mathews et al 2001). The different approaches adopted
in these different studies highlight many of the problems
involved in developing pain assessment schemes (Holton
et al 1998). In their original study, Firth and Haldane (1999)
carried out detailed behavioural assessments of dogs, both
before and after surgery, and identified behaviours that were
probable indicators of pain. However, when these criteria
were used to identify animals that should have been experi-
encing pain (because they had undergone surgery and had
not received an analgesic), the confidence intervals on the
measures were wide. In addition, since only animals under-
going a single type of surgical procedure (ovariohysterecto-
my) were included, the broader applicability of the scheme
cannot be properly evaluated. A different approach was
adopted by Holton et al (2001). This group sought to identify
descriptors of pain by consulting with experienced small
animal clinicians, and then used sophisticated analytical
techniques to reduce these descriptors to a set of words or
phrases. These descriptors were then developed into a
multi-dimensional pain scale. Validation of this scheme, by
using it to correctly identify animals that have received
varying degrees of pain relief following surgery, has not yet
been undertaken. Until this validation has been completed it
is difficult to judge the reliability of the scoring system. It is
hardly surprising that when the scheme is used by clinicians,
whose opinion shaped its development, it successfully
predicts patterns of analgesic use. What is required is a
randomised, blinded, placebo-controlled trial. This, however,
poses certain ethical and practical difficulties (see below).
Despite these problems, this system has been developed fur-
ther and also combined with the Firth and Haldane scheme
to produce a scoring system for clinical use (Hellyer 2002).
Ethical and other problems with pain
assessment schemes
Many other pain scoring schemes have been described, but
virtually none of these has been properly validated. Indeed,
the descriptions of the scales used in some studies are so
brief that it is not possible to make a judgement as to how
useful the scoring system would have been. In general, these
schemes suffer from a number of problems:
(1) The assessment criteria used are frequently highly sub-
jective.
(2) The study design does not include untreated (surgery
and no analgesia) control groups.
(3) The study design does not include anaesthesia and anal-
gesia (and no surgery) control groups.
Since many schemes include some behavioural assessment,
and anaesthetics and analgesics (notably opioids) can
markedly change behaviour in normal, pain-free animals,
the lack of appropriate controls makes the results obtained
highly questionable. However, inclusion of such control
groups can cause significant ethical problems to those
undertaking pain assessment studies. The majority of these
studies are carried out in veterinary schools in which students
are taught that animals experience pain and that analgesics
should therefore be administered. Deliberately withholding
analgesics in circumstances thought likely to result in pain
may therefore be considered unacceptable. This problem is
addressed in studies of pain in human subjects by imple-
menting an intervention analgesia protocol, so that if the
subject is assessed as experiencing pain above a certain
level, they are removed from the study and given an anal-
gesic. This assessment can be carried out by someone not
directly involved in the study. This approach has been used
successfully in a number of veterinary clinical studies
(Lascelles et al 1995; Grisneaux et al 1999) and in labora-
tory animals (Roughan & Flecknell 2003).
Other problems remain, however. In addition to poor study
design, few scales have demonstrated linearity ie is a
score of 4 twice as painful as a score of 2? Furthermore, few
have addressed the problems of between-observer variation
in applying the scoring system. However, it is encouraging
that when placebo controls are included it is possible to
demonstrate significant effects of analgesic administration
(eg Lascelles et al 1997), suggesting that some elements of
the scale used are indicators of pain. Considerable additional
work is required before any of these schemes could be con-
sidered sufficiently reproducible or robust for use in veteri-
nary clinical practice. The assessment schemes have also
examined pain only in dogs and cats pain in birds, rabbits,
small mammals, reptiles, amphibians and fish, all of which
may undergo surgery in veterinary practice, has received
virtually no attention.
Pain assessment in laboratory animals
It might be thought that pain assessment in this group of
animals would be the most highly developed, given the
great public concern regarding their welfare. Although sug-
gestions for assessing pain have been published (Flecknell
© 2004 Universities Federation for Animal Welfare
Assessing pain in animals S73
1984), these were largely based on subjective clinical crite-
ria that had not been subjected to any form of validation. A
proposal to develop more robust scoring schemes was
published by Morton and Griffiths (1985), but attempts to
apply this were largely unsuccessful (Beynen et al 1987),
primarily because the variables selected for inclusion were
not fully identified and because the scales used were not
sufficiently well characterised. The scheme has proven
much more successful when applied as a means of develop-
ing more humane endpoints for experiments (Cussler et al
1999). These problems were identified by the original
authors, but the indiscriminate application of the system
seems to have led to a failure in identifying animals in pain,
and to some research facilities abandoning its application.
This is to be regretted since, when applied carefully, the
scheme provides a structured method for assessing animals
and can be a useful aid for developing endpoints in a range
of different situations.
Other potential indicators of pain in laboratory animals have
included general locomotor activity and changes in food
consumption and body weight (Flecknell & Liles 1991;
Liles & Flecknell 1993; Liles et al 1998). These latter meas-
ures are objective and have been used to assess analgesic
drug efficacy. However, they are retrospective measures and
so cannot be used to modify analgesic therapy for a particular
animal. They can, however, be used as a simple measure of
post-operative recovery, and as a means of adjusting future
analgesic regimens for similar animals undergoing similar
surgical procedures.
Other pain assessment systems have aimed at identifying
acute and chronic pain states for research purposes (eg
DAmour & Smith 1941; Dubuisson & Dennis 1977; Gyires
& Torma 1984), but these have limited application in
assessing pain in other situations. A range of different tech-
niques has been developed for assessing the likely efficacy
of analgesics. In many instances, these involve the applica-
tion of a brief noxious stimulus, followed by quantification
of the animals response. Administration of analgesics usu-
ally modifies this response, for example by prolonging the
latency to withdraw a limb or tail from the noxious stimulus.
In addition to their primary use as a means of screening for
potential analgesics in drug discovery programs, the results
of these tests have been used to estimate dose rates of anal-
gesics for clinical use (Flecknell 1984). However, such
extrapolations must be made with caution. For example,
estimates of appropriate doses of buprenorphine based on
tail flick tests resulted in a recommended dose of
0.5 mg kg1 in rats (Flecknell 1984), which is 10 times high-
er than the dose shown to be effective using post-operative
pain scoring systems (Liles & Flecknell 1993; Flecknell
et al 1999). Since high doses of this agent can have undesir-
able side-effects, it is important that care is taken when
making these extrapolations. Although results of these types
of test may not predict clinical efficacy, they do illustrate the
very wide variation in response that can be encountered
between different strains of rodent (Morgan et al 1999).
This reinforces the importance of developing pain scoring
systems. If appropriate pain scoring schemes cannot be
used, dose rates are probably best estimated from the results
of tonic analgesiometric tests such as the late-phase formalin
test or the writhing test (Roughan & Flecknell 2002).
Recently, we have developed a behaviour-based scheme for
assessing pain in laboratory rats following abdominal sur-
gery (Roughan & Flecknell 2001). During the initial devel-
opment of the scheme, the behaviour of rats was evaluated
following a mid-line laparotomy with appropriate untreated,
and non-surgery analgesic-treated controls being included.
An initial study using buprenorphine as the analgesic was
inconclusive because of the marked effects of this opioid on
normal behaviour (Roughan & Flecknell 2000). A subse-
quent study using carprofen and ketoprofen successfully
identified a series of behaviours that differentiated rats that
had received analgesics following surgery from those that
had not. These studies required detailed analysis of consid-
erable periods of video-taped behaviour, and filming at
night under red light. Therefore, although the scoring criteria
were suitable as a research tool, they did not provide a prac-
tically useful scoring system.
Following this study, the more general utility of the system
was assessed in a different strain of rat undergoing surgery
as part of an unrelated research project. In these studies, the
animals were placed in an observation cage for a 10 min
period and the frequency of pain-related behaviours was
assessed. It proved possible to differentiate animals receiv-
ing analgesics from untreated controls, and to demonstrate a
dose-related effect of the NSAID meloxicam (Roughan &
Flecknell 2003). Re-analysis of all of the behaviours shown
by these rats confirmed that the same behaviours as those
seen in our previous investigations were the most useful for
developing a clinically applicable pain scoring scheme.
When experienced staff (animal technicians, research workers
and veterinarians) viewed selected video recordings from
these animals they were unable to correctly identify the
treatment groups. However, after viewing a short recording
illustrating the key pain-related behaviours, their ability to
identify animals that had, or had not, received analgesics
greatly improved (Roughan & Flecknell in press).
These studies suggested that key behaviours could be iden-
tified and used to score pain following one type of surgical
procedure in rats. Most recently, we have used the scoring
system to assess the relative efficacy of different analgesics
and their duration of action. In addition, the scoring system
has been applied to rats undergoing a different surgical pro-
cedure, bilateral adrenalectomy. These animals perform a
very similar range of behaviours to animals undergoing
laparotomy, but there are differences in the frequency of
particular behaviours, with back-arching being more fre-
quent after mid-line laparotomy and belly-pressing more
frequent after bilateral adrenalectomy. This is similar to the
results of behavioural studies of lambs undergoing different
methods of castration and tail docking (Molony et al 2002),
in that different types of abnormal behaviour are seen after
the different procedures. What is uncertain is whether behav-
ioural changes in rats after various surgical procedures will
Animal Welfare 2004, 13: S71-75
S74 Flecknell and Roughan
differ greatly in type, or whether they will be drawn from a
common group of abnormal, pain-related behaviours.
A further problem that is becoming apparent is that all of the
rats studied during the development of the pain scoring system
were anaesthetised with isoflurane, a very short acting
anaesthetic that results in rapid recovery of consciousness.
When recovery is delayed, or is associated with prolonged
sedation, animals may fail to express pain behaviour. At
present it is not certain whether this is because the animals
are not experiencing pain, or whether the heavy sedation
prevents them from showing signs of pain. The scoring system
may also be influenced by other factors, such as fear and
apprehension, and unexpected variations in behaviour
between different strains of animal may be encountered.
Nevertheless, this approach offers a step forward in devel-
oping a practically useful scoring system for use after at
least some types of surgery in rats. What is not yet known is
whether similar systems can be developed for other labora-
tory species, or whether a similar approach can be used to
develop means of identifying and quantifying other types of
pain in animals, including chronic pain states.
Practical applications
Given the current poor state of our ability to assess pain, it
is unsurprising that the practical application of any of these
pain scoring schemes remains very limited. Considerably
more research is needed to develop appropriate tools for
assessing pain in many species, and it is essential that we
evaluate current schemes critically. If we do not, and they
are promoted widely and then prove to be unreliable, this
will dissuade veterinary clinicians and others involved in
pain management from applying assessment schemes. A
second problem that is emerging is that applying scoring
schemes in either veterinary clinical practices, research
facilities or on farms, will take a significant amount of time.
Taking the assessment scheme for rats as an example, at
least 510 min per animal is required, and subsequent
assessments, for example at 12 h intervals, should be made
in order to monitor the animals adequately. If 20 or 30 ani-
mals are involved, this can easily develop into a full time
role for a member of staff. It is important that such schemes
are developed and promoted however, because if we do not
have a clear means of identifying animal pain, analgesic use
will continue to be restricted.
In farm animal practice there is little information concern-
ing the level of analgesic use generally, and for specific hus-
bandry procedures such as castration, the use of analgesics
remains very low. In companion animal practice the level of
analgesic use is thought to be growing, encouraged by the
launch of a number of new analgesic agents. It is difficult to
assess the overall level of analgesic use in laboratory
species. Although a recent survey indicates that the provi-
sion of post-surgical pain relief may be widespread in the
UK (Hawkins 2002), this survey was of a highly selected
group of facilities and may not reflect practice elsewhere.
Reviewing research publications involving surgery in
rodents highlights some worrying trends analgesic use is
almost never mentioned in some journals, despite the papers
describing invasive surgical procedures. In several recent
publications, the authors stated that analgesics were not
given because the animals showed no apparent signs of pain
(Lawson et al 2001; Labat et al 2002; Grau & Steiniger
2003); this reinforces the need to provide simple methods of
identifying pain.
Although one point emphasised at the outset of this paper
was the need to educate veterinarians and others involved in
pain management, perhaps the need to educate the general
public is even greater. Many of the issues surrounding pain
management have economic dimensions, and consumers
can influence practices by the choices they make. This has
been illustrated recently in Switzerland, where the introduction
of anaesthesia for the castration of piglets has been success-
ful on some farms. This has been linked with education of
the public to accept a higher price for their food on the
understanding that it has been produced at a lower cost to
the animal (U Schatzman 2002, personal communication).
Conclusion
The recent increase in interest in animal pain and its preven-
tion and alleviation is to be welcomed. We must appreciate,
however, that we currently have a very limited ability to
assess pain intensity accurately. This limits our ability to
prevent and alleviate pain. We must strive to develop robust,
practically useful assessment schemes for a wide range of
different animal species. We must do this for different types
of both acute and chronic pain. If we can make progress
towards this goal we will be able to manage animal pain far
more effectively than is possible at present.
Acknowledgements
The authors research work is supported by the Medical
Research Council.
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