The perception of pain by pigs and implications for farm and veterinary practice

Introduction

The “Five Freedoms” (FAWC, 1993) are used widely as a framework for the assessment of animal welfare and the basis of much legislation for animal protection. Whilst not all Freedoms receive universal agreement, “Freedom from pain, injury and disease” is accepted as important by all stakeholders. Pain can be defined as “an unpleasant sensory and emotional experience associated with actual or potential tissue damage” (IASP, 1979). Since both sensory and emotional experiences are subjective to the individual concerned, it is not possible to be certain how pain is experienced by a non-verbal species. However, the similarities in anatomical structures and responses to pain which occur in humans and non-human animals, which share common evolutionary functions, suggest that pain in pigs should be given appropriate consideration. It has been suggested that, since pain has an important biological function in learning to avoid actions and situations where tissue damage might occur, total freedom from pain is neither possible nor desirable. However, extreme or sustained unavoidable pain serves no beneficial function for the individual and should be treated as a serious welfare issue.

In the process of breeding and rearing pigs, some animals can experience pain which compromises their welfare. In some cases, this pain results directly from procedures carried out as a result of management decisions. Widespread examples of these include the castration of male pigs to reduce the risk of boar taint in the meat, the docking of piglets’ tails to reduce the risk of injurious tail biting in later life, the reduction of canine teeth in neonatal piglets to reduce facial damage from sibling competition, the nose-ringing of outdoor sows to reduce pasture destruction, and the ear tagging, tattooing and slap marking of animals for identification purposes. In other cases, the occurrence of pain is not directly attributable to human intervention, but arises from health disorders developed spontaneously by the animals. These include both acute injuries and infections, and more chronic skeletal, respiratory and enteric conditions. The pain associated with such conditions is still poorly understood, and often relies on human analogy. In this paper, the challenges of understanding, practical assessment and alleviation of pain are discussed with reference to different examples of pain-producing situations, highlighting different issues which must be addressed by scientific research and ethical debate.

The assessment of pain

In a survey of UK veterinarians and pig farmers, many respondents indicated that they found it difficult to assess pain in pigs (Ison and Rutherford, 2014). A number of different approaches exist for the assessment of pain in a practical or experimental context (Rutherford, 2002). The most commonly used approaches relate to the behaviour of the animal. Acute pain is characterised by rapid withdrawal response, escape attempts and by distress vocalisations. The future avoidance of situations in which pain occurred provides evidence that they are associated by the animal with a negative emotional state, rather than the behaviours being simple reflex reactions. Longer term pain can also be assessed by changes in behaviour. These changes can vary from behaviours providing protection to the painful region, such as changes in posture and gait when active, to a state of more general lethargy in which any painful movement is avoided. The extent to which such behavioural changes are reversed when analgesics are administered provides a good indication that they are pain-related, especially if such a response occurs in a dose dependent manner (Weary et al., 2006). Furthermore, the negative affective state can be convincingly demonstrated if animals with supposed painful conditions can be trained to self-administer analgesics, and this can give a method to titrate the extent of the pain.

Since animals have evolved to mask visible signs of pain as an anti-predator adaptation, it is easy to underestimate pain when assessing by behavioural change (Anil et al., 2002). To overcome this, recent methodologies have focussed on more subtle changes. These may be whole body changes in demeanour, as studied by Qualitative Behavioural Assessment (QBA) methods (Wemelsfelder and Lawrence, 2001), or specific changes in facial expression (Grimace Scales), first developed for the study of pain in human infants and subsequently extended to a range of other species including pigs (Di Giminiani et al., 2016a). Because of the masking of spontaneous behavioural signs of pain, an alternative approach is to study evoked responses. The inflammatory responses associated with pain may induce hyperalgesia or allodynia. The heightened sensitivity can be quantified by changes in nociceptive threshold to mechanical or thermal stimulation. This forms the basis of the widely used veterinary diagnostic procedure of palpation of suspected painful areas, but also more controlled experimental use of pressure algometers or lasers (Di Giminiani et al., 2013).

Physiological assessment of pain has often been based on activation of the hypothalamic-pituitary-adrenal axis or of the sympathetic nervous system – the so-called “fight or flight” response. Increased circulating levels of cortisol or adrenaline, or their physiological consequences such as heart, respiration rate or body temperature have been monitored (Lonardi et al., 2015). However, these are somewhat non-specific responses, indicating increased arousal rather than pain per se. While potentially indicative of the extent of a negative affective state in a pain-producing situation, they have a component of fear or anxiety which is present even in the absence of any physical stimulus. Other blood constituents like endorphins or lactate have also been used as pain markers, but none are unambiguous in interpretation. It is known that the relative magnitude of behavioural and physiological responses to welfare challenge may vary between individuals according to the coping strategy they adopt (Koolhaas et al., 1999), which is dependent on both genetic predisposition and early life experience. For this reason, a multifactorial approach to pain assessment involving both behavioural and physiological methods is preferable. However, the behavioural and physiological methods used in the assessment of acute pain may be of little value in assessing persistent but less intense pain. The occurrence of such chronic pain is perhaps the least well understood welfare issue. Newer molecular approaches are helping in the understanding of this (Hunt and Mantyh, 2001), with measurement of changes in expression of genes associated with neural pain pathways now providing evidence of the experience of long term pain.

All of these methodologies are now being applied to current welfare issues within pig production to inform the ethical debate on the acceptability of husbandry practices, to evaluate the efficacy of anaesthesia and analgesia to mitigate the pain associated with such practices if deemed essential, and to assess the desirability of pain relieving interventions in a range of disease states.

Pain associated with husbandry procedures

Castration of male piglets is a pain-causing procedure widely carried out to avoid the risk of undesirable odour and flavour in the meat from compounds associated with male sexual development (the so-called “boar taint”), which markedly reduces the value of the carcass. Whilst animal welfare benefits may also arise, through reduction in aggression and undesirable sexual behaviours as animals reach puberty, it has been shown in experimental studies and large scale practice that intact males can be reared without major welfare problems when management is good. The justification for the procedure can thus be considered as largely for human economic benefit and ethical considerations demand that the need for the practice should be questioned and, if it is considered necessary, that methods to prevent or alleviate any associated pain should be sought. Historically, castration has been carried out on the young piglet without anaesthesia or analgesia. There is no doubt that this procedure causes intense pain during the surgery itself, and that some degree of discomfort persists for several days (von Borell et al., 2009). Given this knowledge, the necessity for the procedure is a topic of current debate. Some countries (UK, Ireland) have largely abolished the practice and other countries are moving in this direction (Backus et al., 2014). This has been stimulated by the 2010 European declaration on alternatives to surgical castration of pigs, a voluntary agreement between stakeholders which states that surgical castration of pigs should be abandoned by 1 January 2018. Whilst progress towards achieving this goal has been made through genetic selection and nutritional interventions to reduce boar taint, and through development of rapid methods for taint detection and on-line carcass sorting, there is uncertainty about how soon these can deliver an acceptable system for entire male production. There are also particular production systems for specialised products, e.g. the heavy pigs for Italian ham production and traditional breeds in organic and silvo-pastoral rearing systems, where use of entire males may still be infeasible. As an interim measure in many countries, and a possible longer term solution in specialist systems, the continuation of surgical castration with prolonged analgesia and/or anaesthesia is being implemented. Whilst injectable analgesia is simpler to apply, and thus the preferred practical option in most countries at the present time, scientific evidence suggests that it is unable to reliably abolish the acute pain experienced during surgery. In several countries, general anaesthesia is, or will soon become, a legal requirement for continuation of surgical castration but the difficulty and cost of this approach make others doubtful about application. The alternative approach of immunological castration is now technically feasible, and implemented in some countries, but gives rise to significant consumer and retailer concerns. Even if these can be overcome, the ethical issue of animal integrity still remains a barrier to any approach except entire male production.

Tail docking is also a deliberate management procedure but, unlike castration, its justification is argued on the basis of a cost/benefit balance for the animal itself. It is carried out on the young piglet to reduce the risk of receiving injury from tail biting in later life, which is unquestionably a serious welfare problem. Tail docking also differs from castration in the degree of pain apparently associated with the procedure, with many farmers believing this to be negligible on the basis of the piglet reactions that they observe. Whilst more detailed scientific study suggests that acute pain does indeed occur (Lonardi et al., 2013), and a difference in expression of Crhr1 mRNA in the amygdala, a molecular marker of anxiety, was detectable at 10 days after neonatal docking (Oberst et al., 2015), other measurements of stress physiology have sometimes shown effects no greater than distress from the handling process (Edwards and Bennett, 2014). However, neuromas which occur as a result of repair processes in injured peripheral nerves in the docked tail (Sandercock et al., 2016a) have been suggested to cause altered peripheral nerve activity that may cause pain or chronic discomfort. Whilst significant uncertainty still exists about this question, it has been shown that, although tails damaged in later life show a prolonged increase in sensitivity, there is no evidence that this is the case following neonatal docking (Di Giminiani et al., 2016b). Furthermore, the molecular markers indicative of changes in peripheral and spinal nociceptive processing associated with possible inflammatory and chronic pain appear to resolve by 4 weeks after tail docking injury (Sandercock et al., 2016b). If it can be demonstrated that long term pain does not occur, and that any acute and medium term pain can be alleviated by appropriate use of anaesthesia and analgesia, then the welfare implications of the procedure for the animal itself might be minimal and justifiable to reduce risk of the far greater harm of being tail bitten. However, this does not remove the ethical argument for respecting the integrity of animals. Some countries have already abolished tail docking and, whilst the prevalence of tail biting is higher than in docked animals, risk can be minimised by appropriate housing and management. The risk factors for tail biting have been widely studied and tools for risk evaluation and risk reduction now exist (Taylor et al., 2012). However, even with systems deemed to be of low risk, significant tail biting outbreaks can still occur and, in the absence of any reliable method to control their severity once started, many farmers are reluctant to accept such risk. Looking to the future, genetic selection strategies and improvement in enrichment provision offer further risk reduction potential, whilst recent work on the neuroendocrine basis of tail biting may lead to pharmacological control products which could make this reduced risk acceptable in commercial practice.

Even lesser procedures, including ear tagging and ear notching, have now been shown by multidisciplinary assessment methods to cause significant acute pain and merit analgesia (Leslie et al., 2010). Whilst greatest societal and scientific attention has been focussed on the pain associated with deliberate management procedures, from the perspective of the animals these may not be the most important sources of pain-induced welfare compromise. The pain associated with procedures is primarily acute and predictable in time, and therefore amenable to planned pain control interventions. This contrasts with the possibility for both acute and chronic pain associated with unpredictable, and possibly undetected, health conditions.

Pain associated with disease states

The pain associated with lameness arising from trauma, infection or degenerative joint disease is now starting to receive more scientific attention (Jensen et al., 2012). Lameness can be characterised by alteration in gait (Stavrakakis et al., 2015), and these gait alterations can be reduced by administration of analgesics in both sows (Conte et al., 2016) and growing pigs (Meijer et al., 2015) indicating that they are truly reflective of pain. However, the potential for pain associated with other endemic conditions is still relatively neglected. Oesophago-gastric ulcers have been shown in a number of surveys to be widespread in both growing pigs and sows. They are characterised by erosion and ulceration of the lining of the stomach. As they become more severe, intermittent bleeding may take place leading to anaemia and, in extreme cases, massive haemorrhage and death (Friendship, 2006). As many as 60-80% of growing pigs can show some degree of alteration or erosion of the stomach lining, and 5-10% have more serious ulceration. In sows the problem seems even greater, with 25% or more of animals showing ulceration. The extent to which these ulcers cause pain to affected animals in relation to their degree of severity is unknown, although only animals with more severe ulcers show inappetance and loss of condition. In humans, the condition is known to be acutely painful, and the similarity in anatomy might suggest this to also be the case in pigs. If so, the high prevalence of the condition constitutes a serious welfare problem. However, since no reliable diagnostics have been validated in live animals, it is difficult to assess the time course of ulcer development and current degree of severity in order to evaluate the extent of any associated pain and address remediation. Similarly, although pneumonia and pleurisy cause significant chest pain in humans (Kass et al., 2007), a literature search suggests that the extent of this issue in pigs awaits scientific investigation.

Conclusions

The occurrence of pain in pig production compromises animal welfare and must be actively addressed. Where such pain arises from deliberate management decisions, an ethical justification needs to be underpinned by objective scientific assessment of the intensity and duration of pain and distress associated with each course of action. This assessment can be problematic, as our understanding of the subjective experience of pain in animals is still lacking, and multidisciplinary assessment methodologies need to be employed. The assessment of chronic pain is particularly challenging, making it difficult to quantify for endemic health disorders which may have widespread prevalence. Whilst the principal goal must be to remove the sources of pain through modification of production practice and reduction in known risk factors, this will not always be completely effective. A reliable method for on-farm pain assessment is then an essential prerequisite for effective alleviation by appropriate anaesthesia and analgesia, and is a pressing subject for research.

Presented at the 24th International Pig Veterinary Society Congress. For information on the next edition, click here.