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Facial pain expression
Practice Points
Kenneth M Prkachin† People in pain from various causes often show a characteristic facial expression. The expression consists mainly of eye closure, brow lowering, contraction of the levator labii muscle and,
especially, contraction of the orbicularis oculi, narrowing the eye opening and raising the cheeks. The expression encodes pain intensity, but is not inevitable. Observers of the pain expression typically underestimate the intensity of pain that it conveys: it should
be thought of as a ‘late’ signal – if it is there it is more intense than you may think. High levels of exposure to facial expressions of pain appear to bias observers against perceiving pain.
This may explain why some healthcare professionals show an exaggerated underestimation bias. The clinical implications of pain underestimation are not known and should be the focus of increased
attention and research.
SUMMARY
People in pain communicate their experience via facial expressions. There has been considerable research into the properties of pain expressions. This article reviews basic findings on the encoding and decoding of pain expression. The facial expression of pain is characterized and recent findings on its assessment and psychometric properties are described. Studies on decoding of pain expression are also reviewed, focusing on observers’ sensitivity to and bias in evaluation of pain expression. Priority areas for future research are identified. We cannot know another person’s pain directly. Yet, it is common for people to draw inferences about other people’s pain. A parent needs to know whether to keep a child home from school, an emergency responder needs to determine which victim is in greatest need of help, a coach needs to know when a player returning from injury should be returned to the lineup, and so on. In the clinic, a geriatrician wishes to ensure that a nonverbal patient is comfortable or a pediatrician considers whether pain
control intervention is needed for a premature neonate. Although there are problems with the inferences that people draw in such circumstances, we are often able to identify when another person is in pain without sharing his or her consciousness. The existence of such intersubjectivity indicates, first, that people who are suffering provide perceptible evidence to that effect and, second, that there must be some correspondence between evidence of suffering and the subjective state.
Department of Psychology, University of Northern British Columbia, 3333 University Way, Prince George, BC, N2L 3G1, Canada; Tel.: +1 250 960 6633; Fax: +1 250 960 5744; [email protected] †
10.2217/PMT.11.22 © 2011 Future Medicine Ltd
Pain Manage. (2011) 1(4), 367–376
ISSN 1758-1869
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Review Prkachin The evidence for knowing another’s pain comes primarily from the sufferer’s behavior. There is, of course, a venerable tradition seeking insight into others’ pain by measurement of nonbehavioral variables such as autonomic responses, changes in electroencephalographic activity and more recent neuroimaging techniques. But such methods are limited with respect to the question of how we can know the pain of another. The behaviors that convey information about pain are diverse but fall into distinct categories. The most salient exist in visual and auditory domains: withdrawing an afflicted limb, bracing or rubbing a part of the body, facial grimaces, moaning, groaning, crying out in agony, or, at the greatest level of complexity, using words to describe the experience, sometimes with great precision. It remains to be seen whether significant information about human pain is conveyed in other sensory modalities. All such behaviors are communicative in the sense that they indicate that a person is in pain, which is why they are often subsumed under the rubric ‘pain behaviors’ [1] . But that appellation glosses over important fundamental distinctions [2,3] . Behaviors like withdrawing a hand from a hot stove are escape or avoidance behaviors. They are communicative, but only indirectly. We know through observation that these are things that people do when tissue damage has happened or is expected to happen, but they are primarily adaptive behaviors. They control the immediate situation, contributing to self-protection and ultimately survival. Rubbing or limping are pain-control behaviors that minimize suffering and promote healing. Behaviors like using visual analog scales to quantify the unpleasantness of a noxious stimulus or a clinical condition are indeed directly communicative but serve other multiple functions and may communicate things other than pain [4] . Of all these behaviors, facial expressions are particularly interesting from a communication perspective. They do not play a direct role in modulating pain. Rather, the human capacity to encode pain coevolved with the capacity to decode it [5,6] . This article provides a brief review of the current status of our understanding of the facial expression of pain from the perspectives of encoding and decoding. Encoding pain The idea that there is a specific facial signal that registers information about pain may seem selfevident, yet, with a few exceptions, there was
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little interest in it through the greater part of the 19th and 20th centuries. This paralleled trends in psychology in which the zeitgeist until approximately the 1970s was that facial expressions are socially determined and culturally specific and therefore provide only context-dependent information about internal states. This zeitgeist was supported by early empirical studies which also appeared to indicate that detection of internal states by facial expression was crude [7] . The zeitgeist began to change in the 1970s as a result of developments in the study of emotion; in particular, the work of Ekman [8] showing that facial expressions of particular emotions could be recognized cross-culturally. These findings prompted considerable rethinking of the psychology of emotion and a new interest in the face as a vehicle for communicating about internal states. A related methodological development was probably of even greater significance. Human facial expressions are extraordinarily complex and difficult to study with scientific objectivity and precision. Attempts to develop systems for measuring facial expressions met with little success; in part because the descriptions of facial actions involved in expressions were subjective, dependent on varying human judgments and often required inferences about the very internal states they were intended to measure. A measurement standard for facial expressions eluded scientific consensus. In 1978, Ekman and Friesen published their attempt to resolve this problem in the form of the Facial Action Coding System (FACS) [9] . FACS is a measurement system that is based on ‘decomposition’ of visible facial actions by observers trained to recognize the distinctive appearance changes caused by the facial muscles. Any perceptible movement of the face can be described in terms of 44 separate actions. FACS also provides a means of quantifying the intensity of most of those distinct actions. Importantly, the system is almost purely descriptive, circumventing the problem of inferring the underlying meaning of actions. The emergence of FACS also coincided with the increasing availability of inexpensive video recording equipment, facilitating experimental and observational studies that would allow analysis of the properties of facial behavior in the context of pain. Several of the earliest FACS studies, using candid photographs of people who could be inferred to be in severe pain [10] , experimental pain induced by cold [11] or electric shock [12]
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Facial pain expression and exacerbation of clinical pain [13] identified a subset of actions that could be shown to occur with increased frequency or intensity during pain. Prkachin [14] used FACS to examine facial actions associated with experimentally induced pain in four modalities: cold, pressure, ischemia and electric shock. Integrated with previous findings it was suggested that the facial expression of pain could be quantified in a single index by summing the intensities of four actions that are reliably associated across studies with pain: brow lowering (primarily reflecting action of the corrugator muscle), orbit tightening (reflecting two actions of the orbicularis oculi), nose-wrinkling/ lip raising (reflecting two actions of the levator labii superioris) and eye closure. In some studies, other actions have also been associated with pain; in particular, action of the zygomatic major which is also the principal action involved in smiling, risorius, which draws the lip corners horizontally and the action of opening the mouth. Analyses of the psychometric structure of measurements of all these actions provide strong evidence, however, that brow-lowering, orbit tightening, nose-wrinkling/lip raising and eye closure represent a principal, independent and unified response to painful events [15] . An artist’s portrayal of this expression is presented in Figure 1. Studies of neonates and children, which have made use of hybrid behavioral observation systems similar to FACS, have identified a
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comparable set of actions. In neonates, the pain of heel-lancing procedures is associated with brow bulging, eye squeezing, nasolabial furrow deepening, lip parting and a taut, cupped tongue [16] . In children, the pain of surgery and immunizations has been associated with cheek raising, nasolabial furrow deepening, vertical mouth stretching, brow lowering, squinting, nose wrinkling and eye squeezing, all actions that are consistent with the characterization of pain expression in adults, as described using FACS [17,18] . Likewise, elderly people exposed to pain produced by mechanical and electrical stimulation showed increased orbit tightening, levator contraction and brow lowering [19] . This evidence of homology of pain expression across the lifespan and across widely divergent pain modalities provides considerable reason to believe that there is a unified, ‘core’ expression of pain, addressing two criteria for considering an expression to be universal. A third criterion for universality – consistency across cultures – has yet to be addressed systematically. To date, all studies reported used participants from developed, western cultures. Although many have had samples that reflect the ethnic and ‘racial’ diversity of the locales in which they have been conducted, none have focused on what could be called ‘traditional’ cultures or cultures having had minimal exposure to western influences and none have made ethnic/’racial’ differences a dimension of analysis. This is a
Figure 1. Artist’s rendering of emergence of the core pain expression movements over time. The rendering is from a video recording of a patient with shoulder pathology moving the affected limb through a range of motion. (A) The action begins to be perceptible, with lowering of the brows, narrowing of the eyes and appearance of the nasolabial furrow. (B) Brow lowering, eyelid narrowing, cheek raising and appearance of action of the levator labii superioris are clear. (C) Eye closure is superimposed on the aforementioned movements, with clear tightening of the eyelids as the movement reaches maximum intensity. Reproduced with permission from [14].
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Review Prkachin significant shortcoming because of the widespread belief in profound cultural differences in pain expression, an idea supported by early sociological studies [20] . If pain expression has properties that resemble those of emotional expressions, it is likely that evidence in support of both universality and cultural differences will emerge. Indeed, based on the neurocultural theory of emotion [7] it is possible to hypothesize that there will be universality in the form of pain expression, but cross-cultural variability in the circumstances of its appearance. In other words, when pain is expressed it will look the same, but the extent to which it is expressed or self‑regulated will vary across cultures. The fact that the actions described as a core expression vary systematically and strongly with conditions that clearly relate to differences in pain provides strong evidence supporting construct validity and use of the term ‘pain expression’. Other evidence supports concurrent validity. In particular, sound psychometric studies have shown that the pain expression correlates with self-reports of pain intensity [12,15,21] . Likewise, in patients suffering from low back pain, facial expressions during a physical examination were correlated with a range of other pain behaviors, including guarding, rubbing, nonverbal vocalizations, complaining and quantitative self-reports of pain, and with clinicians’ ratings of the overall amount of pain displayed [22] . While the FACS has provided an important method for characterizing the facial expression of pain and articulating its properties, the system has major shortcomings: it is laborious and requires the expertise of highly trained human observers. This has limited its application in both discovery and clinical contexts. Given, however, that enough is known to be able to characterize a core pain expression, it is possible to construct systems that reduce the burden of observation considerably, making application in clinical contexts feasible. For example, using a system based on recognizing and quantifying its components, Prkachin et al. [23] trained observers to perform real-time assessment of pain expression in a sample of subacute low back pain patients undergoing a clinical examination. The observers were able to perform the assessments reliably and the measurements were predictive of other indicators of pain intensity [22] . Likewise, Grunau et al. [24] have demonstrated the feasibility of bedside application of their system for coding pain expression in neonates.
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It can be argued that the burden of assessing pain expression outweighs its potential value either as a vehicle for discovery about pain mechanisms or an approach to clinical assessment. What is the point of such a procedure if there are perfectly adequate alternatives, such as verbal reports, commonly considered the ‘gold standard’ of pain assessment? There are at least two answers to this criticism. The first is that it is clear that whatever information is being provided by pain expression, it is different from that which comes from verbal reports and other measurement techniques. Studies that have examined relationships between facial expression and self-report measures show intercorrelations that are, for the most part, modest. More important, however, is that assessment of pain expression can uncover evidence about first-person pain processes that other, more commonly used measures, cannot. For example, Kunz et al. [25] examined facial and verbal pain responses to variations in pressure pain intensity among patients with dementia and matched controls. They reported a precise dose–response relationship between pressure pain and pain expression that was enhanced among patients with dementia, whose expressions indicated greater pain than controls’. Many patients could not use verbal ratings to describe their pain, while among those who could, there were no differences from controls. These are important findings because they reveal a distinct difference in the processing of pain among patients with dementia that is inconsistent with prevailing beliefs about pain in this population. They also show that, at least in this instance, more traditional measures were not sufficiently sensitive to be informative. Similar findings of paradoxically enhanced pain responsiveness in populations with developmental disabilities have been revealed with facial measurement [26] . It should be noted, however, that there are populations in which the facial response to pain has been shown to be blunted or unreliable, such as adolescents with neurological impairments [27] . Likewise, in certain specific pain syndromes involving the face itself, such as trigeminal neuralgia, interpretation of facial actions in terms of pain expression may be unwarranted. The emerging field of affective computing [28] holds promise to transform both the assessment of pain expression and our understanding of its properties. Assessing pain
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Facial pain expression expression is essentially a problem of pattern recognition: if there is a specific configuration of facial changes that signal pain, then application of computer vision techniques that identify facial features, track their movement and model changes may allow us to design artificial systems to approximate the perception of human experts. Remarkable progress has been made using techniques of automated facial analysis to identify movements involved in facial expressions of emotion [29] . More recently, Ashraf et al. [30] directly examined the ability of an automatic analysis system to distinguish videos of patients when they were known to be experiencing pain or not. A system making use of the technique of active appearance models coupled with the use of support vector machines to distinguish individual video frames displaying pain achieved a hit rate of 82% and a false affirmative rate of 30%. Figure 2 shows this system applied to frameby-frame changes in the facial expression of one patient during an episode of pain expression. Note how the system not only identifies and circumscribes the episode, but also allows tracking of dynamic temporal and intensive changes in the expression. Such fine-grained representation of the properties of the facial action is virtually impossible to achieve with human observers.
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Since there is reason to believe that such parameters of the pain expression as their intensity and features of temporal change (duration, rise-time, decay time) may be informative about the neuropsychological processes affecting the suffering individual [31] , these techniques appear to have the potential to advance our knowledge of pain processes significantly. At a practical level, they may also hold the potential to develop useful clinical assessment tools, such as remote monitoring for pain. Decoding pain Several authors have emphasized that pain expression is one component of a social communication process [2,5,6,32,33] . Accordingly, a complete understanding of the nature, determinants and implications of pain expression requires consideration of how people perceive pain expression. People are certainly adept at detecting when others are in pain by observing pain expression. When people watch recordings of pain expression under highly controlled circumstances, they are remarkably sensitive [34] . This sensitivity is present from an early age [35] and appears to be preserved even among people who have diminished experience with first-person pain such as patients afflicted
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Figure 2. Example of automatic analysis of the pain expression of a patient with shoulder pathology. The figure shows the output of an automatic analysis system, displaying on the ordinate a prediction function representing a prediction of pain. The abscissa represents time in video frames. Specific video images associated with individual frames are also depicted. Reproduced with permisison from [30]. The photos were originally published in Image and Vision Computing, with the patient’s consent.
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Review Prkachin with congenital insensitivity to pain [36] . Recent neuroimaging studies comparing activation of cerebral regions when people are exposed to firstperson pain and third-person pain in the form of recordings of natural pain expressions have identified commonalities in regions activated; particularly in anterior cingulate and insular cortex [37] . These findings are consistent with the perception-action model of empathy, which suggests that emotional intersubjectivity is dependent at some level on correspondence between the neural structures subserving direct perception of events and our representation of those events in ourselves and others [38] . From an evolutionary perspective one might argue that this ability is adaptive because it supports our ability to identify others who are in peril from bodily injury and come to their assistance [39] , but it is not at all clear that the only adaptive response to evidence of suffering in others is to come to their aid. It is not difficult to imagine circumstances in which evidence of pain in another may signal peril to the observer or even more sinister scenarios that could set the stage for escape, ignoring or even aggression on the part of the observer. Features of the decoding of pain expression are of particular interest in the context of clinical assessment. Ever since the initial popularization of the concept of pain behavior some three to four decades ago (e.g., [40]), clinicians have acknowledged the importance of attending to the ways in which people express their pain. Nevertheless, consensus about how to interpret pain expression does not exist. Consider the following quotation from a medical-legal report on a low back pain patient: “Throughout the assessment the client did not display … facial grimacing … [This] leads [me] to believe that the … primary reason for self limiting may be – fear of re-injury.” The expectation seems to be that if the patient’s difficulties were being driven primarily by pain, one should observe pain expression. By contrast, consider the following conclusion by a different clinician about a different patient: “During today’s … assessment, significant pain magnifying features [pain expressions] were observed. Such a presentation is thought to be due to acquired overprotective behaviors.” In this case, the expectation seems to be that the existence of pain expressions is an indication that something other than pain is the primary determinant. Thus, substantially different interpretations are made of the same
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domain of evidence. This variability is common in clinical settings, underscores the limits of the explicit or implicit theories we use to make sense of pain expression and emphasizes the need for further research to diminish our pretences to knowledge [41] . A distinction can be made between sensitivity to pain expression and the ability to estimate another’s pain. Sensitivity refers to the ability to recognize that another person is showing pain. It implies nothing about how closely the observer’s judgment may match the experience of the sufferer. The ability to estimate refers to the degree of correspondence between an observer’s and a sufferer’s judgment of the sufferer’s pain. Despite the fact that people are generally quite sensitive to pain expression, their ability to estimate others’ pain with precision has generally been found to be problematic. For example, Prkachin et al. had judges observe video recordings of the pain expressions of shoulder pain patients [42] . The patients had rated their own pain and the judges used the same verbal report scales to rate the patients’ pain. Judges ratings were some 50–80% lower than patients’. This ‘underestimation bias’ has been documented in a number of studies and can be demonstrated when the observer’s task is to estimate a sufferer’s pain based on pain expression or other forms of evidence [43] . In some respects, it should not be surprising that observers underestimate others’ pain. After all, we have no direct window into others’ experience and must base our estimates on whatever evidence is at hand. When the available evidence is pain expression, the actions that indicate pain are often small and subtle. Studies using FACS to measure the facial reaction to experimental pain have shown that often people show little or no facial activity even when reporting intolerable pain. It seems likely that this reflects two limitations inherent in studies of experimental pain. First, experimental studies almost always take place in a social context that involves the presence of strangers. As Williams has pointed out, these are circumstances that, in adult humans, are most likely to produce deliberate inhibition of expressive behavior [6] . Second, in experimental studies people volunteer, and there are strict limits to the intensity of pain it is possible to administer ethically. By contrast, it has also been shown that volunteers instructed to suppress facial expressions of pain are, to a statistically significant degree,
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Facial pain expression unsuccessful [44,45] . These observations suggest that the facial expression should be considered a “late signaling system” [5] . The implication is that under ordinary circumstances, if there is evidence of pain on the face, it is likely that the experience of the sufferer is significant. Nevertheless, the underestimation bias is a phenomenon of substantial interest because it may be informative about the social nexus between pain sufferers and those around them. For example, Prkachin et al. compared the judgments of shoulder pain patients’ pain of two groups of observers, each of which had significant experience with people suffering from pain, and the judgments of people who had had little to no experience with pain sufferers [46] . The groups who had had experience with pain sufferers were healthcare professionals with experience treating pain patients and family members of chronic pain patients. Observers based their judgments on video recordings of the pain expressions of patients going through rangeof-motion exercises and used the same rating scales the patients had used. All three groups of observers’ ratings were significantly lower than the patients’, demonstrating the general underestimation bias. However, there was differentiation in the nature of the underestimation bias. Observers who had had family members with chronic pain demonstrated reduced bias – their estimates were closer to the patients’ than controls’ estimates. By contrast, the healthcare professionals with experience treating pain sufferers demonstrated an exaggerated bias – their ratings were even lower than the controls’. Similar findings of enhanced underestimation among professional groups have been reported when the basis provided for judgment is other than pain expression [43] , suggesting that it is not an isolated phenomenon. The concept of a third-person underestimation bias is certainly consistent with the reports of pain patients from whom it is common to hear that they feel that their pain is being ignored or discounted. Consequently, it is worthy of serious inquiry. To date, however, there has been little in the way of systematic investigation of the determinants of this bias and even less of its implications. One potential source that has been investigated is the sheer density of exposure to evidence of pain. In an experimental study, Prkachin et al. showed observers brief excerpts of patients showing facial expressions of moderate pain or no pain [47] . Four groups varied in
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terms of the amount of preceding exposure to recordings depicting strong pain expressions. There was a linear relationship between the amount of exposure and the likelihood of judging the patients to be in pain: the more exposure to pain expression, the more unwilling observers were to judge the test stimuli as involving pain. This finding, which has since been replicated [34] , suggests a relatively benign interpretation of enhanced underestimation among healthcare professionals. The theory of adaptation level [48] holds that perceptual judgments in multiple sensory dimensions are relative and strongly influenced by what one is used to. If people are frequently exposed to stimuli of high intensity, then new evidence will be evaluated against a relatively high standard. Health professionals who work with pain sufferers certainly are exposed to both a high frequency of pain expression and a range of pain produced by injuries that can be extreme. To the extent that this ‘recalibrates’ the individual, underestimation would be a predictable consequence. Another potential determinant of the underestimation effect derives from evolutionary psychology. Pain expressions play a role in access to ‘social entitlements’. A person who communicates that he or she is in pain may be comforted, cared for or given access to benefits contingent on their status as a sufferer. It is, of course, possible to display pain quite convincingly, even if one is not suffering [44,45,49] . If a person can gain access to the same benefits by displaying pain, even though they are not suffering, evolutionary psychology holds that systems for ‘cheater detection’ would also likely have evolved [6] . It is certainly true that in clinical practice, medico-legal processes and folk psychology the idea that people may use pain to achieve outcomes to which they are not entitled is not uncommon. Kappesser et al. studied this concept experimentally by showing health professionals recordings of pain expressions and asking them to rate the patients’ pain using the same rating scales that the patients used [50] . In one condition, the observers were only shown pain expressions. In a second, they were shown the pain expressions and told what the patient’s actual rating was. The third condition was the same as the second with the addition of information that the patients were seeking opioid medication. Observers who only viewed pain expressions showed significant and substantial underestimation, relative to the patients. When
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Review Prkachin given the patients’ actual pain ratings, underestimation was virtually eliminated. However, the addition of information implicating opioid use was enough to virtually reinstate the underestimation bias, eliminating the benefit obtained by providing the patients’ actual ratings. Moreover, the higher the professionals’ base-rate estimates of the amount of pain exaggeration that occurs, the greater the underestimation, regardless of condition. These findings suggest that something very like a ‘cheater detection’ mechanism operates and, when invoked, can be an important determinant of pain underestimation. The foregoing findings suggest that both experience and cognitive activity related to pain and suffering can have a significant influence on the amount of pain people impute to others when they observe pain expression. They only scratch the surface of imaginable influences, however, and are incomplete in themselves. For example, it may be possible to explain exaggerated underestimation among healthcare professionals by invoking the experimental finding that high rates of exposure make people unwilling to impute pain to others. The same observation cannot, however, adequately account for the observation of diminished underestimation among other groups (family members) who also have high exposure to evidence of pain. If these group differences are valid, then something quite different must underlie them. What is clear, however, is that the perception of others’ pain based on pain expression, and any other effect that is dependent on such perception, including, ultimately, what to do about it is highly malleable. Although we are learning more about the perception of others’ pain and future research will undoubtedly add depth and precision to this understanding, there remains an important area of investigation that is virtually unexplored. This is the question of the long-term impact of the perception of pain expression in the lives of people subjected to such judgments. There is certainly reason to believe that the responses of people who are insensitive to evidence of pain or who tend to diminish its intensity will be different from the responses of people who are more sensitive or who give higher estimates of its intensity. Such responses may play a role in child-rearing and other forms of social influence, with long-term effects on those who are exposed to them. At a more practical level, a
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strong argument can be made that the impact of styles of perception of others’ pain should be the focus of active research in clinical settings. For example, is underestimation bias a positive or a negative factor in terms of health outcomes for pain sufferers or for health professionals themselves? Different theoretical positions and ideologies could support varying expectations. It is certainly true, however, that pain patients themselves frequently identify others’ (mis)perceptions of their pain as a source not only of personal distress but also of poor clinical outcomes. On the other hand, underestimation, for example, may be associated with improved outcomes. The current state of knowledge is insufficient to give anything close to a reasonable answer, a situation that urgently needs to be rectified. Conclusion The facial expression of pain has been the focus of a substantial amount of research in the past 30 years and significant progress has been made in understanding its properties. There is evidence for a distinct facial signal that accompanies pain. It does not bear a one-to-one relationship with the pain experience, and it can be affected by personal characteristics, disease processes, social factors and cultural factors. Nevertheless, it is informative about people’s pain experiences, sometimes in ways that other pain indicators cannot be and in some cases, such as in people with limited verbal communication skills, indispensible. Studies have revealed that there are problems in the ways that observers perceive pain expressions, such as the underestimation bias. There is reason to believe that such problems may affect clinical treatment and outcomes but, at present, there is an insufficient base of evidence to draw definitive conclusions, justifying a need for more research in this area. Financial & competing interests disclosure The author’s research reported in this article has been supported by the Canadian Institutes of Health Research and the Social Sciences and Humanities Research Council of Canada. The author has no other relevant affiliations or financial involvement with any organization or entity with a financial interest in or financial conflict with the subject matter or materials discussed in the manuscript apart from those disclosed. No writing assistance was utilized in the production of this manuscript.
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Facial pain expression Bibliography 1
2
3
4
5
6
Keefe FJ, Williams DA, Smith SJ. Assessment of pain behaviors. In Handbook of Pain Assessment (2nd Edition). Turk DC, Melzack R (Eds). Guilford, NY, USA, 170–187 (2001). Hadjistavropoulos T, Craig KD. A theoretical framework for understanding self-report and observational measures of pain: a communications model. Behav. Res. Ther. 40, 551–570 (2002). Sullivan MJL. Toward a biopsychomotor conceptualization of pain: implications for research and intervention. Clin. J. Pain 24, 281–290 (2008). Williams AC de C, Davies HTO, Chadury Y. Simple pain rating scales hide complex idiosyncratic meanings. Pain 85, 457–463 (2000). Prkachin KM, Craig KD. Expressing pain: the communication and interpretation of facial pain signals. J. Nonverbal Behav. 19, 191–205 (1994). Williams AC de C. Facial expression of pain: an evolutionary account. Behav. Brain Sci. 25, 439–488 (2002).
7
Ekman P. Emotion in the Human Face (2nd Edition). Cambridge University Press, New York, NY, USA (1982).
8
Ekman P, Friesen WV. Constants across cultures in the face and emotion. J. Pers. Soc. Psychol. 17, 124–129 (1971).
9
10
11
Ekman P, Friesen WV. Manual for the Facial Action Coding System. Consulting Psychologists Press, Palo Alto, CA, USA (1978). LeResche L. Facial expression in pain: a survey of candid photographs. J. Nonverbal Behav. 7, 45–56 (1982). Craig KD, Patrick CJ. Facial expression during induced pain. J. Pers. Soc. Psychol. 48, 1080–1091 (1985).
12 Patrick CJ, Craig KD, Prkachin KM.
Observer judgements of acute pain: facial action determinants. J. Pers. Soc. Psychol. 50, 1291–1298 (1986). 13 Prkachin KM, Mercer S. Pain expression in
patients with shoulder pathology: validity, coding properties and relation to sickness impact. Pain 39, 257–265 (1989). 14
Prkachin KM. The consistency of facial expressions of pain: a comparison across modalities. Pain 51, 297–306 (1992).
15
Prkachin KM, Solomon PE. The structure, reliability and validity of pain expression: evidence from patients with shoulder pain. Pain 139, 267–274 (2008).
future science group
16
17
18
19
Grunau RVE, Craig KD. Pain expression in neonates: facial action and cry. Pain 28, 395–410 (1987). Breau LM, McGrath PJ, Craig KD, Santor D, Cassidy K-L, Reid GJ. Facial expression of children receiving immunizations: a principal components analysis of the Child Facial Coding System. Clin. J. Pain 17, 178–186 (2001). Gilbert CA, Lilley CM, Craig KD et al. Postoperative pain expression in preschool childen: validation of the child facial coding system. Clin. J. Pain 15, 192–200 (1999). Kunz M, Mylius V, Schepelmann K, Lautenbacher S. Impact of age on the facial expression of pain. J. Psychosomat. Res. 64, 311–318 (2008).
20 Zborowski M. Cultural components in
29 Cohn JF, Ekman PE. Measuring facial action.
In: The New Handbook of Methods in Nonverbal Behavior Research. Harrigan JA, Rosenthal R, Scherer KR (Eds). Oxford University Press, New York, NY, USA, 9–64 (2005). 30 Ashraf AB, Lucey S, Cohn JF et al. The
painful face – pain expression recognition using active appearance models. Image Vis. Comput. 27, 1788–1796 (2009). 31
Kunz M, Mylius V, Schepelmann K, Lautenbacher S. On the relationship between self-report and facial expression of pain. J. Pain 5, 368–376 (2004).
model of pain. Can. Psychol. 50, 22–32 (2009). 33 Sullivan MJL, Adams H, Sullivan ME.
Communicative dimensions of pain catastrophizing: social cueing effects on pain behaviour and coping. Pain 107, 220–226 (2004). 34 Prkachin KM, Rocha EM. High levels of
vicarious exposure bias pain judgments. J. Pain 11, 904–909 (2010).
22 Prkachin KM, Schultz I, Berkowitz J,
Hughes E, Hunt D. Assessing pain behaviour in real time: concurrent validity and examiner sensitivity. Behav. Res. Ther. 40, 595–607 (2002). 23 Prkachin KM, Hughes EA, Schultz I, Joy P,
Hunt D. Real-time assessment of pain behavior during clinical assessment of low-back pain patients. Pain 95, 23–30 (2002). 24 Grunau RVE, Oberlander T, Holsti L,
Winfield MF. Bedside application of the Neonatal Facial Coding System in pain assessment of premature neonates. Pain 76, 277–286 (1998). 25 Kunz M, Scharmann S, Hemmeter U,
Schepelmann K, Lautenbacher S. The facial expression of pain in patients with dementia. Pain 133, 221–228 (2007). 26 Symons FJ, Harper V, Shinde SK, Clary J,
Bodfish JW. Evaluating a sham-controlled sensory-testing protocol for nonverbal adults with neurodevelopmental disorders: self-injury and gender effects. J. Pain 8, 773–781 (2010). 27 Oberlander TF, Gilbert C, Chambers CT,
O’Donnell ME, Craig KD. Biobehavioral responses to acute pain in adolescents with a significant neurological impairment. Clin. J. Pain 15, 201–209 (1999). 28 Pickard RW. Affective Computing.
MIT Press, Cambridge, MA, USA (1997).
Rinn WE. The neuropsychology of facial expression: a review of the neurological and psychological mechanisms for producing facial expressions. Psychol. Bull. 95, 52–77 (1982).
32 Craig KD. The social communication
response to pain. J. Social Issues 8, 16–30 (1952). 21
Review
35
Deyo K, Prkachin KM, Mercer SR. Development of sensitivity to facial expressions of pain. Pain 107, 16–21 (2004).
36 Danziger N, Prkachin KM, Willer J-C.
Is pain the price to pay to feel empathy? Brain 129, 2494–2507 (2006). 37 Botvinick M, Jha AP, Bylsma LM, Fabian SA,
Solomon PE, Prkachin KM. Viewing facial expressions of pain engages cortical areas involved in the direct experience of pain. Neuroimage 25, 312–319 (2005). 38 Preston SD, de Waal FBM. Empathy:
its ultimate and proximate bases. Behav. Brain Sci. 25, 1–20 (2002). 39 Prkachin KM. Pain behaviour is not unitary.
Behav. Brain Sci. 9, 754–755 (1986). 40 Fordyce WE. Behavioral Methods for Chronic
Pain and Illness. Mosby, St Louis, MO, USA (1976). 41 Prkachin KM. Pain behavior and the pretence
of knowledge. Behav. Brain Sci. 25, 470 (2002). 42 Prkachin KM, Berzins S, Mercer S.
Encoding and decoding of pain expressions: a judgement study. Pain 58, 253–259 (1994). 43 Prkachin KM, Solomon PA, Ross AJ.
The underestimation of pain among healthcare providers. Can. J. Nurs. Res. 39, 88–106 (2007).
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Review Prkachin 44 Craig KD, Hyde SA, Patrick CJ. Genuine,
suppressed and faked facial behavior during exacerbation of low back pain. Pain 46, 161–171 (1991). 45
Prkachin KM. Effects of deliberate control on verbal and facial expressions of pain. Pain 114, 328–338 (2005).
46 Prkachin KM, Solomon P, Hwang T,
Mercer SR. Does experience affect judgements of pain behaviour? Evidence from relatives of pain patients and healthcare providers. Pain Res. Manag. 6, 105–112 (2001). 47 Prkachin KM, Mass H, Mercer SR. Effects of
exposure on perception of pain expression. Pain 111, 8–12 (2004).
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Pain Manage. (2011) 1(4)
48 Helson H. Adaptation-Level Theory.
Harper & Row, New York, NY, USA (1964). 49 Prkachin KM. Dissociating deliberate and
spontaneous expressions of pain. Pain 51, 57–65 (1992). 50 Kappesser J, Williams AC de C,
Prkachin KM. Testing two accounts of pain underestimation. Pain 124, 109–116 (2006).
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Facial pain expression
Practice Points
Kenneth M Prkachin† People in pain from various causes often show a characteristic facial expression. The expression consists mainly of eye closure, brow lowering, contraction of the levator labii muscle and,
especially, contraction of the orbicularis oculi, narrowing the eye opening and raising the cheeks. The expression encodes pain intensity, but is not inevitable. Observers of the pain expression typically underestimate the intensity of pain that it conveys: it should
be thought of as a ‘late’ signal – if it is there it is more intense than you may think. High levels of exposure to facial expressions of pain appear to bias observers against perceiving pain.
This may explain why some healthcare professionals show an exaggerated underestimation bias. The clinical implications of pain underestimation are not known and should be the focus of increased
attention and research.
SUMMARY
People in pain communicate their experience via facial expressions. There has been considerable research into the properties of pain expressions. This article reviews basic findings on the encoding and decoding of pain expression. The facial expression of pain is characterized and recent findings on its assessment and psychometric properties are described. Studies on decoding of pain expression are also reviewed, focusing on observers’ sensitivity to and bias in evaluation of pain expression. Priority areas for future research are identified. We cannot know another person’s pain directly. Yet, it is common for people to draw inferences about other people’s pain. A parent needs to know whether to keep a child home from school, an emergency responder needs to determine which victim is in greatest need of help, a coach needs to know when a player returning from injury should be returned to the lineup, and so on. In the clinic, a geriatrician wishes to ensure that a nonverbal patient is comfortable or a pediatrician considers whether pain
control intervention is needed for a premature neonate. Although there are problems with the inferences that people draw in such circumstances, we are often able to identify when another person is in pain without sharing his or her consciousness. The existence of such intersubjectivity indicates, first, that people who are suffering provide perceptible evidence to that effect and, second, that there must be some correspondence between evidence of suffering and the subjective state.
Department of Psychology, University of Northern British Columbia, 3333 University Way, Prince George, BC, N2L 3G1, Canada; Tel.: +1 250 960 6633; Fax: +1 250 960 5744; [email protected] †
10.2217/PMT.11.22 © 2011 Future Medicine Ltd
Pain Manage. (2011) 1(4), 367–376
ISSN 1758-1869
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Review Prkachin The evidence for knowing another’s pain comes primarily from the sufferer’s behavior. There is, of course, a venerable tradition seeking insight into others’ pain by measurement of nonbehavioral variables such as autonomic responses, changes in electroencephalographic activity and more recent neuroimaging techniques. But such methods are limited with respect to the question of how we can know the pain of another. The behaviors that convey information about pain are diverse but fall into distinct categories. The most salient exist in visual and auditory domains: withdrawing an afflicted limb, bracing or rubbing a part of the body, facial grimaces, moaning, groaning, crying out in agony, or, at the greatest level of complexity, using words to describe the experience, sometimes with great precision. It remains to be seen whether significant information about human pain is conveyed in other sensory modalities. All such behaviors are communicative in the sense that they indicate that a person is in pain, which is why they are often subsumed under the rubric ‘pain behaviors’ [1] . But that appellation glosses over important fundamental distinctions [2,3] . Behaviors like withdrawing a hand from a hot stove are escape or avoidance behaviors. They are communicative, but only indirectly. We know through observation that these are things that people do when tissue damage has happened or is expected to happen, but they are primarily adaptive behaviors. They control the immediate situation, contributing to self-protection and ultimately survival. Rubbing or limping are pain-control behaviors that minimize suffering and promote healing. Behaviors like using visual analog scales to quantify the unpleasantness of a noxious stimulus or a clinical condition are indeed directly communicative but serve other multiple functions and may communicate things other than pain [4] . Of all these behaviors, facial expressions are particularly interesting from a communication perspective. They do not play a direct role in modulating pain. Rather, the human capacity to encode pain coevolved with the capacity to decode it [5,6] . This article provides a brief review of the current status of our understanding of the facial expression of pain from the perspectives of encoding and decoding. Encoding pain The idea that there is a specific facial signal that registers information about pain may seem selfevident, yet, with a few exceptions, there was
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little interest in it through the greater part of the 19th and 20th centuries. This paralleled trends in psychology in which the zeitgeist until approximately the 1970s was that facial expressions are socially determined and culturally specific and therefore provide only context-dependent information about internal states. This zeitgeist was supported by early empirical studies which also appeared to indicate that detection of internal states by facial expression was crude [7] . The zeitgeist began to change in the 1970s as a result of developments in the study of emotion; in particular, the work of Ekman [8] showing that facial expressions of particular emotions could be recognized cross-culturally. These findings prompted considerable rethinking of the psychology of emotion and a new interest in the face as a vehicle for communicating about internal states. A related methodological development was probably of even greater significance. Human facial expressions are extraordinarily complex and difficult to study with scientific objectivity and precision. Attempts to develop systems for measuring facial expressions met with little success; in part because the descriptions of facial actions involved in expressions were subjective, dependent on varying human judgments and often required inferences about the very internal states they were intended to measure. A measurement standard for facial expressions eluded scientific consensus. In 1978, Ekman and Friesen published their attempt to resolve this problem in the form of the Facial Action Coding System (FACS) [9] . FACS is a measurement system that is based on ‘decomposition’ of visible facial actions by observers trained to recognize the distinctive appearance changes caused by the facial muscles. Any perceptible movement of the face can be described in terms of 44 separate actions. FACS also provides a means of quantifying the intensity of most of those distinct actions. Importantly, the system is almost purely descriptive, circumventing the problem of inferring the underlying meaning of actions. The emergence of FACS also coincided with the increasing availability of inexpensive video recording equipment, facilitating experimental and observational studies that would allow analysis of the properties of facial behavior in the context of pain. Several of the earliest FACS studies, using candid photographs of people who could be inferred to be in severe pain [10] , experimental pain induced by cold [11] or electric shock [12]
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Facial pain expression and exacerbation of clinical pain [13] identified a subset of actions that could be shown to occur with increased frequency or intensity during pain. Prkachin [14] used FACS to examine facial actions associated with experimentally induced pain in four modalities: cold, pressure, ischemia and electric shock. Integrated with previous findings it was suggested that the facial expression of pain could be quantified in a single index by summing the intensities of four actions that are reliably associated across studies with pain: brow lowering (primarily reflecting action of the corrugator muscle), orbit tightening (reflecting two actions of the orbicularis oculi), nose-wrinkling/ lip raising (reflecting two actions of the levator labii superioris) and eye closure. In some studies, other actions have also been associated with pain; in particular, action of the zygomatic major which is also the principal action involved in smiling, risorius, which draws the lip corners horizontally and the action of opening the mouth. Analyses of the psychometric structure of measurements of all these actions provide strong evidence, however, that brow-lowering, orbit tightening, nose-wrinkling/lip raising and eye closure represent a principal, independent and unified response to painful events [15] . An artist’s portrayal of this expression is presented in Figure 1. Studies of neonates and children, which have made use of hybrid behavioral observation systems similar to FACS, have identified a
Review
comparable set of actions. In neonates, the pain of heel-lancing procedures is associated with brow bulging, eye squeezing, nasolabial furrow deepening, lip parting and a taut, cupped tongue [16] . In children, the pain of surgery and immunizations has been associated with cheek raising, nasolabial furrow deepening, vertical mouth stretching, brow lowering, squinting, nose wrinkling and eye squeezing, all actions that are consistent with the characterization of pain expression in adults, as described using FACS [17,18] . Likewise, elderly people exposed to pain produced by mechanical and electrical stimulation showed increased orbit tightening, levator contraction and brow lowering [19] . This evidence of homology of pain expression across the lifespan and across widely divergent pain modalities provides considerable reason to believe that there is a unified, ‘core’ expression of pain, addressing two criteria for considering an expression to be universal. A third criterion for universality – consistency across cultures – has yet to be addressed systematically. To date, all studies reported used participants from developed, western cultures. Although many have had samples that reflect the ethnic and ‘racial’ diversity of the locales in which they have been conducted, none have focused on what could be called ‘traditional’ cultures or cultures having had minimal exposure to western influences and none have made ethnic/’racial’ differences a dimension of analysis. This is a
Figure 1. Artist’s rendering of emergence of the core pain expression movements over time. The rendering is from a video recording of a patient with shoulder pathology moving the affected limb through a range of motion. (A) The action begins to be perceptible, with lowering of the brows, narrowing of the eyes and appearance of the nasolabial furrow. (B) Brow lowering, eyelid narrowing, cheek raising and appearance of action of the levator labii superioris are clear. (C) Eye closure is superimposed on the aforementioned movements, with clear tightening of the eyelids as the movement reaches maximum intensity. Reproduced with permission from [14].
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Review Prkachin significant shortcoming because of the widespread belief in profound cultural differences in pain expression, an idea supported by early sociological studies [20] . If pain expression has properties that resemble those of emotional expressions, it is likely that evidence in support of both universality and cultural differences will emerge. Indeed, based on the neurocultural theory of emotion [7] it is possible to hypothesize that there will be universality in the form of pain expression, but cross-cultural variability in the circumstances of its appearance. In other words, when pain is expressed it will look the same, but the extent to which it is expressed or self‑regulated will vary across cultures. The fact that the actions described as a core expression vary systematically and strongly with conditions that clearly relate to differences in pain provides strong evidence supporting construct validity and use of the term ‘pain expression’. Other evidence supports concurrent validity. In particular, sound psychometric studies have shown that the pain expression correlates with self-reports of pain intensity [12,15,21] . Likewise, in patients suffering from low back pain, facial expressions during a physical examination were correlated with a range of other pain behaviors, including guarding, rubbing, nonverbal vocalizations, complaining and quantitative self-reports of pain, and with clinicians’ ratings of the overall amount of pain displayed [22] . While the FACS has provided an important method for characterizing the facial expression of pain and articulating its properties, the system has major shortcomings: it is laborious and requires the expertise of highly trained human observers. This has limited its application in both discovery and clinical contexts. Given, however, that enough is known to be able to characterize a core pain expression, it is possible to construct systems that reduce the burden of observation considerably, making application in clinical contexts feasible. For example, using a system based on recognizing and quantifying its components, Prkachin et al. [23] trained observers to perform real-time assessment of pain expression in a sample of subacute low back pain patients undergoing a clinical examination. The observers were able to perform the assessments reliably and the measurements were predictive of other indicators of pain intensity [22] . Likewise, Grunau et al. [24] have demonstrated the feasibility of bedside application of their system for coding pain expression in neonates.
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It can be argued that the burden of assessing pain expression outweighs its potential value either as a vehicle for discovery about pain mechanisms or an approach to clinical assessment. What is the point of such a procedure if there are perfectly adequate alternatives, such as verbal reports, commonly considered the ‘gold standard’ of pain assessment? There are at least two answers to this criticism. The first is that it is clear that whatever information is being provided by pain expression, it is different from that which comes from verbal reports and other measurement techniques. Studies that have examined relationships between facial expression and self-report measures show intercorrelations that are, for the most part, modest. More important, however, is that assessment of pain expression can uncover evidence about first-person pain processes that other, more commonly used measures, cannot. For example, Kunz et al. [25] examined facial and verbal pain responses to variations in pressure pain intensity among patients with dementia and matched controls. They reported a precise dose–response relationship between pressure pain and pain expression that was enhanced among patients with dementia, whose expressions indicated greater pain than controls’. Many patients could not use verbal ratings to describe their pain, while among those who could, there were no differences from controls. These are important findings because they reveal a distinct difference in the processing of pain among patients with dementia that is inconsistent with prevailing beliefs about pain in this population. They also show that, at least in this instance, more traditional measures were not sufficiently sensitive to be informative. Similar findings of paradoxically enhanced pain responsiveness in populations with developmental disabilities have been revealed with facial measurement [26] . It should be noted, however, that there are populations in which the facial response to pain has been shown to be blunted or unreliable, such as adolescents with neurological impairments [27] . Likewise, in certain specific pain syndromes involving the face itself, such as trigeminal neuralgia, interpretation of facial actions in terms of pain expression may be unwarranted. The emerging field of affective computing [28] holds promise to transform both the assessment of pain expression and our understanding of its properties. Assessing pain
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Facial pain expression expression is essentially a problem of pattern recognition: if there is a specific configuration of facial changes that signal pain, then application of computer vision techniques that identify facial features, track their movement and model changes may allow us to design artificial systems to approximate the perception of human experts. Remarkable progress has been made using techniques of automated facial analysis to identify movements involved in facial expressions of emotion [29] . More recently, Ashraf et al. [30] directly examined the ability of an automatic analysis system to distinguish videos of patients when they were known to be experiencing pain or not. A system making use of the technique of active appearance models coupled with the use of support vector machines to distinguish individual video frames displaying pain achieved a hit rate of 82% and a false affirmative rate of 30%. Figure 2 shows this system applied to frameby-frame changes in the facial expression of one patient during an episode of pain expression. Note how the system not only identifies and circumscribes the episode, but also allows tracking of dynamic temporal and intensive changes in the expression. Such fine-grained representation of the properties of the facial action is virtually impossible to achieve with human observers.
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Since there is reason to believe that such parameters of the pain expression as their intensity and features of temporal change (duration, rise-time, decay time) may be informative about the neuropsychological processes affecting the suffering individual [31] , these techniques appear to have the potential to advance our knowledge of pain processes significantly. At a practical level, they may also hold the potential to develop useful clinical assessment tools, such as remote monitoring for pain. Decoding pain Several authors have emphasized that pain expression is one component of a social communication process [2,5,6,32,33] . Accordingly, a complete understanding of the nature, determinants and implications of pain expression requires consideration of how people perceive pain expression. People are certainly adept at detecting when others are in pain by observing pain expression. When people watch recordings of pain expression under highly controlled circumstances, they are remarkably sensitive [34] . This sensitivity is present from an early age [35] and appears to be preserved even among people who have diminished experience with first-person pain such as patients afflicted
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Figure 2. Example of automatic analysis of the pain expression of a patient with shoulder pathology. The figure shows the output of an automatic analysis system, displaying on the ordinate a prediction function representing a prediction of pain. The abscissa represents time in video frames. Specific video images associated with individual frames are also depicted. Reproduced with permisison from [30]. The photos were originally published in Image and Vision Computing, with the patient’s consent.
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Review Prkachin with congenital insensitivity to pain [36] . Recent neuroimaging studies comparing activation of cerebral regions when people are exposed to firstperson pain and third-person pain in the form of recordings of natural pain expressions have identified commonalities in regions activated; particularly in anterior cingulate and insular cortex [37] . These findings are consistent with the perception-action model of empathy, which suggests that emotional intersubjectivity is dependent at some level on correspondence between the neural structures subserving direct perception of events and our representation of those events in ourselves and others [38] . From an evolutionary perspective one might argue that this ability is adaptive because it supports our ability to identify others who are in peril from bodily injury and come to their assistance [39] , but it is not at all clear that the only adaptive response to evidence of suffering in others is to come to their aid. It is not difficult to imagine circumstances in which evidence of pain in another may signal peril to the observer or even more sinister scenarios that could set the stage for escape, ignoring or even aggression on the part of the observer. Features of the decoding of pain expression are of particular interest in the context of clinical assessment. Ever since the initial popularization of the concept of pain behavior some three to four decades ago (e.g., [40]), clinicians have acknowledged the importance of attending to the ways in which people express their pain. Nevertheless, consensus about how to interpret pain expression does not exist. Consider the following quotation from a medical-legal report on a low back pain patient: “Throughout the assessment the client did not display … facial grimacing … [This] leads [me] to believe that the … primary reason for self limiting may be – fear of re-injury.” The expectation seems to be that if the patient’s difficulties were being driven primarily by pain, one should observe pain expression. By contrast, consider the following conclusion by a different clinician about a different patient: “During today’s … assessment, significant pain magnifying features [pain expressions] were observed. Such a presentation is thought to be due to acquired overprotective behaviors.” In this case, the expectation seems to be that the existence of pain expressions is an indication that something other than pain is the primary determinant. Thus, substantially different interpretations are made of the same
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domain of evidence. This variability is common in clinical settings, underscores the limits of the explicit or implicit theories we use to make sense of pain expression and emphasizes the need for further research to diminish our pretences to knowledge [41] . A distinction can be made between sensitivity to pain expression and the ability to estimate another’s pain. Sensitivity refers to the ability to recognize that another person is showing pain. It implies nothing about how closely the observer’s judgment may match the experience of the sufferer. The ability to estimate refers to the degree of correspondence between an observer’s and a sufferer’s judgment of the sufferer’s pain. Despite the fact that people are generally quite sensitive to pain expression, their ability to estimate others’ pain with precision has generally been found to be problematic. For example, Prkachin et al. had judges observe video recordings of the pain expressions of shoulder pain patients [42] . The patients had rated their own pain and the judges used the same verbal report scales to rate the patients’ pain. Judges ratings were some 50–80% lower than patients’. This ‘underestimation bias’ has been documented in a number of studies and can be demonstrated when the observer’s task is to estimate a sufferer’s pain based on pain expression or other forms of evidence [43] . In some respects, it should not be surprising that observers underestimate others’ pain. After all, we have no direct window into others’ experience and must base our estimates on whatever evidence is at hand. When the available evidence is pain expression, the actions that indicate pain are often small and subtle. Studies using FACS to measure the facial reaction to experimental pain have shown that often people show little or no facial activity even when reporting intolerable pain. It seems likely that this reflects two limitations inherent in studies of experimental pain. First, experimental studies almost always take place in a social context that involves the presence of strangers. As Williams has pointed out, these are circumstances that, in adult humans, are most likely to produce deliberate inhibition of expressive behavior [6] . Second, in experimental studies people volunteer, and there are strict limits to the intensity of pain it is possible to administer ethically. By contrast, it has also been shown that volunteers instructed to suppress facial expressions of pain are, to a statistically significant degree,
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Facial pain expression unsuccessful [44,45] . These observations suggest that the facial expression should be considered a “late signaling system” [5] . The implication is that under ordinary circumstances, if there is evidence of pain on the face, it is likely that the experience of the sufferer is significant. Nevertheless, the underestimation bias is a phenomenon of substantial interest because it may be informative about the social nexus between pain sufferers and those around them. For example, Prkachin et al. compared the judgments of shoulder pain patients’ pain of two groups of observers, each of which had significant experience with people suffering from pain, and the judgments of people who had had little to no experience with pain sufferers [46] . The groups who had had experience with pain sufferers were healthcare professionals with experience treating pain patients and family members of chronic pain patients. Observers based their judgments on video recordings of the pain expressions of patients going through rangeof-motion exercises and used the same rating scales the patients had used. All three groups of observers’ ratings were significantly lower than the patients’, demonstrating the general underestimation bias. However, there was differentiation in the nature of the underestimation bias. Observers who had had family members with chronic pain demonstrated reduced bias – their estimates were closer to the patients’ than controls’ estimates. By contrast, the healthcare professionals with experience treating pain sufferers demonstrated an exaggerated bias – their ratings were even lower than the controls’. Similar findings of enhanced underestimation among professional groups have been reported when the basis provided for judgment is other than pain expression [43] , suggesting that it is not an isolated phenomenon. The concept of a third-person underestimation bias is certainly consistent with the reports of pain patients from whom it is common to hear that they feel that their pain is being ignored or discounted. Consequently, it is worthy of serious inquiry. To date, however, there has been little in the way of systematic investigation of the determinants of this bias and even less of its implications. One potential source that has been investigated is the sheer density of exposure to evidence of pain. In an experimental study, Prkachin et al. showed observers brief excerpts of patients showing facial expressions of moderate pain or no pain [47] . Four groups varied in
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terms of the amount of preceding exposure to recordings depicting strong pain expressions. There was a linear relationship between the amount of exposure and the likelihood of judging the patients to be in pain: the more exposure to pain expression, the more unwilling observers were to judge the test stimuli as involving pain. This finding, which has since been replicated [34] , suggests a relatively benign interpretation of enhanced underestimation among healthcare professionals. The theory of adaptation level [48] holds that perceptual judgments in multiple sensory dimensions are relative and strongly influenced by what one is used to. If people are frequently exposed to stimuli of high intensity, then new evidence will be evaluated against a relatively high standard. Health professionals who work with pain sufferers certainly are exposed to both a high frequency of pain expression and a range of pain produced by injuries that can be extreme. To the extent that this ‘recalibrates’ the individual, underestimation would be a predictable consequence. Another potential determinant of the underestimation effect derives from evolutionary psychology. Pain expressions play a role in access to ‘social entitlements’. A person who communicates that he or she is in pain may be comforted, cared for or given access to benefits contingent on their status as a sufferer. It is, of course, possible to display pain quite convincingly, even if one is not suffering [44,45,49] . If a person can gain access to the same benefits by displaying pain, even though they are not suffering, evolutionary psychology holds that systems for ‘cheater detection’ would also likely have evolved [6] . It is certainly true that in clinical practice, medico-legal processes and folk psychology the idea that people may use pain to achieve outcomes to which they are not entitled is not uncommon. Kappesser et al. studied this concept experimentally by showing health professionals recordings of pain expressions and asking them to rate the patients’ pain using the same rating scales that the patients used [50] . In one condition, the observers were only shown pain expressions. In a second, they were shown the pain expressions and told what the patient’s actual rating was. The third condition was the same as the second with the addition of information that the patients were seeking opioid medication. Observers who only viewed pain expressions showed significant and substantial underestimation, relative to the patients. When
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Review Prkachin given the patients’ actual pain ratings, underestimation was virtually eliminated. However, the addition of information implicating opioid use was enough to virtually reinstate the underestimation bias, eliminating the benefit obtained by providing the patients’ actual ratings. Moreover, the higher the professionals’ base-rate estimates of the amount of pain exaggeration that occurs, the greater the underestimation, regardless of condition. These findings suggest that something very like a ‘cheater detection’ mechanism operates and, when invoked, can be an important determinant of pain underestimation. The foregoing findings suggest that both experience and cognitive activity related to pain and suffering can have a significant influence on the amount of pain people impute to others when they observe pain expression. They only scratch the surface of imaginable influences, however, and are incomplete in themselves. For example, it may be possible to explain exaggerated underestimation among healthcare professionals by invoking the experimental finding that high rates of exposure make people unwilling to impute pain to others. The same observation cannot, however, adequately account for the observation of diminished underestimation among other groups (family members) who also have high exposure to evidence of pain. If these group differences are valid, then something quite different must underlie them. What is clear, however, is that the perception of others’ pain based on pain expression, and any other effect that is dependent on such perception, including, ultimately, what to do about it is highly malleable. Although we are learning more about the perception of others’ pain and future research will undoubtedly add depth and precision to this understanding, there remains an important area of investigation that is virtually unexplored. This is the question of the long-term impact of the perception of pain expression in the lives of people subjected to such judgments. There is certainly reason to believe that the responses of people who are insensitive to evidence of pain or who tend to diminish its intensity will be different from the responses of people who are more sensitive or who give higher estimates of its intensity. Such responses may play a role in child-rearing and other forms of social influence, with long-term effects on those who are exposed to them. At a more practical level, a
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strong argument can be made that the impact of styles of perception of others’ pain should be the focus of active research in clinical settings. For example, is underestimation bias a positive or a negative factor in terms of health outcomes for pain sufferers or for health professionals themselves? Different theoretical positions and ideologies could support varying expectations. It is certainly true, however, that pain patients themselves frequently identify others’ (mis)perceptions of their pain as a source not only of personal distress but also of poor clinical outcomes. On the other hand, underestimation, for example, may be associated with improved outcomes. The current state of knowledge is insufficient to give anything close to a reasonable answer, a situation that urgently needs to be rectified. Conclusion The facial expression of pain has been the focus of a substantial amount of research in the past 30 years and significant progress has been made in understanding its properties. There is evidence for a distinct facial signal that accompanies pain. It does not bear a one-to-one relationship with the pain experience, and it can be affected by personal characteristics, disease processes, social factors and cultural factors. Nevertheless, it is informative about people’s pain experiences, sometimes in ways that other pain indicators cannot be and in some cases, such as in people with limited verbal communication skills, indispensible. Studies have revealed that there are problems in the ways that observers perceive pain expressions, such as the underestimation bias. There is reason to believe that such problems may affect clinical treatment and outcomes but, at present, there is an insufficient base of evidence to draw definitive conclusions, justifying a need for more research in this area. Financial & competing interests disclosure The author’s research reported in this article has been supported by the Canadian Institutes of Health Research and the Social Sciences and Humanities Research Council of Canada. The author has no other relevant affiliations or financial involvement with any organization or entity with a financial interest in or financial conflict with the subject matter or materials discussed in the manuscript apart from those disclosed. No writing assistance was utilized in the production of this manuscript.
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Facial pain expression Bibliography 1
2
3
4
5
6
Keefe FJ, Williams DA, Smith SJ. Assessment of pain behaviors. In Handbook of Pain Assessment (2nd Edition). Turk DC, Melzack R (Eds). Guilford, NY, USA, 170–187 (2001). Hadjistavropoulos T, Craig KD. A theoretical framework for understanding self-report and observational measures of pain: a communications model. Behav. Res. Ther. 40, 551–570 (2002). Sullivan MJL. Toward a biopsychomotor conceptualization of pain: implications for research and intervention. Clin. J. Pain 24, 281–290 (2008). Williams AC de C, Davies HTO, Chadury Y. Simple pain rating scales hide complex idiosyncratic meanings. Pain 85, 457–463 (2000). Prkachin KM, Craig KD. Expressing pain: the communication and interpretation of facial pain signals. J. Nonverbal Behav. 19, 191–205 (1994). Williams AC de C. Facial expression of pain: an evolutionary account. Behav. Brain Sci. 25, 439–488 (2002).
7
Ekman P. Emotion in the Human Face (2nd Edition). Cambridge University Press, New York, NY, USA (1982).
8
Ekman P, Friesen WV. Constants across cultures in the face and emotion. J. Pers. Soc. Psychol. 17, 124–129 (1971).
9
10
11
Ekman P, Friesen WV. Manual for the Facial Action Coding System. Consulting Psychologists Press, Palo Alto, CA, USA (1978). LeResche L. Facial expression in pain: a survey of candid photographs. J. Nonverbal Behav. 7, 45–56 (1982). Craig KD, Patrick CJ. Facial expression during induced pain. J. Pers. Soc. Psychol. 48, 1080–1091 (1985).
12 Patrick CJ, Craig KD, Prkachin KM.
Observer judgements of acute pain: facial action determinants. J. Pers. Soc. Psychol. 50, 1291–1298 (1986). 13 Prkachin KM, Mercer S. Pain expression in
patients with shoulder pathology: validity, coding properties and relation to sickness impact. Pain 39, 257–265 (1989). 14
Prkachin KM. The consistency of facial expressions of pain: a comparison across modalities. Pain 51, 297–306 (1992).
15
Prkachin KM, Solomon PE. The structure, reliability and validity of pain expression: evidence from patients with shoulder pain. Pain 139, 267–274 (2008).
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16
17
18
19
Grunau RVE, Craig KD. Pain expression in neonates: facial action and cry. Pain 28, 395–410 (1987). Breau LM, McGrath PJ, Craig KD, Santor D, Cassidy K-L, Reid GJ. Facial expression of children receiving immunizations: a principal components analysis of the Child Facial Coding System. Clin. J. Pain 17, 178–186 (2001). Gilbert CA, Lilley CM, Craig KD et al. Postoperative pain expression in preschool childen: validation of the child facial coding system. Clin. J. Pain 15, 192–200 (1999). Kunz M, Mylius V, Schepelmann K, Lautenbacher S. Impact of age on the facial expression of pain. J. Psychosomat. Res. 64, 311–318 (2008).
20 Zborowski M. Cultural components in
29 Cohn JF, Ekman PE. Measuring facial action.
In: The New Handbook of Methods in Nonverbal Behavior Research. Harrigan JA, Rosenthal R, Scherer KR (Eds). Oxford University Press, New York, NY, USA, 9–64 (2005). 30 Ashraf AB, Lucey S, Cohn JF et al. The
painful face – pain expression recognition using active appearance models. Image Vis. Comput. 27, 1788–1796 (2009). 31
Kunz M, Mylius V, Schepelmann K, Lautenbacher S. On the relationship between self-report and facial expression of pain. J. Pain 5, 368–376 (2004).
model of pain. Can. Psychol. 50, 22–32 (2009). 33 Sullivan MJL, Adams H, Sullivan ME.
Communicative dimensions of pain catastrophizing: social cueing effects on pain behaviour and coping. Pain 107, 220–226 (2004). 34 Prkachin KM, Rocha EM. High levels of
vicarious exposure bias pain judgments. J. Pain 11, 904–909 (2010).
22 Prkachin KM, Schultz I, Berkowitz J,
Hughes E, Hunt D. Assessing pain behaviour in real time: concurrent validity and examiner sensitivity. Behav. Res. Ther. 40, 595–607 (2002). 23 Prkachin KM, Hughes EA, Schultz I, Joy P,
Hunt D. Real-time assessment of pain behavior during clinical assessment of low-back pain patients. Pain 95, 23–30 (2002). 24 Grunau RVE, Oberlander T, Holsti L,
Winfield MF. Bedside application of the Neonatal Facial Coding System in pain assessment of premature neonates. Pain 76, 277–286 (1998). 25 Kunz M, Scharmann S, Hemmeter U,
Schepelmann K, Lautenbacher S. The facial expression of pain in patients with dementia. Pain 133, 221–228 (2007). 26 Symons FJ, Harper V, Shinde SK, Clary J,
Bodfish JW. Evaluating a sham-controlled sensory-testing protocol for nonverbal adults with neurodevelopmental disorders: self-injury and gender effects. J. Pain 8, 773–781 (2010). 27 Oberlander TF, Gilbert C, Chambers CT,
O’Donnell ME, Craig KD. Biobehavioral responses to acute pain in adolescents with a significant neurological impairment. Clin. J. Pain 15, 201–209 (1999). 28 Pickard RW. Affective Computing.
MIT Press, Cambridge, MA, USA (1997).
Rinn WE. The neuropsychology of facial expression: a review of the neurological and psychological mechanisms for producing facial expressions. Psychol. Bull. 95, 52–77 (1982).
32 Craig KD. The social communication
response to pain. J. Social Issues 8, 16–30 (1952). 21
Review
35
Deyo K, Prkachin KM, Mercer SR. Development of sensitivity to facial expressions of pain. Pain 107, 16–21 (2004).
36 Danziger N, Prkachin KM, Willer J-C.
Is pain the price to pay to feel empathy? Brain 129, 2494–2507 (2006). 37 Botvinick M, Jha AP, Bylsma LM, Fabian SA,
Solomon PE, Prkachin KM. Viewing facial expressions of pain engages cortical areas involved in the direct experience of pain. Neuroimage 25, 312–319 (2005). 38 Preston SD, de Waal FBM. Empathy:
its ultimate and proximate bases. Behav. Brain Sci. 25, 1–20 (2002). 39 Prkachin KM. Pain behaviour is not unitary.
Behav. Brain Sci. 9, 754–755 (1986). 40 Fordyce WE. Behavioral Methods for Chronic
Pain and Illness. Mosby, St Louis, MO, USA (1976). 41 Prkachin KM. Pain behavior and the pretence
of knowledge. Behav. Brain Sci. 25, 470 (2002). 42 Prkachin KM, Berzins S, Mercer S.
Encoding and decoding of pain expressions: a judgement study. Pain 58, 253–259 (1994). 43 Prkachin KM, Solomon PA, Ross AJ.
The underestimation of pain among healthcare providers. Can. J. Nurs. Res. 39, 88–106 (2007).
www.futuremedicine.com
375
Review Prkachin 44 Craig KD, Hyde SA, Patrick CJ. Genuine,
suppressed and faked facial behavior during exacerbation of low back pain. Pain 46, 161–171 (1991). 45
Prkachin KM. Effects of deliberate control on verbal and facial expressions of pain. Pain 114, 328–338 (2005).
46 Prkachin KM, Solomon P, Hwang T,
Mercer SR. Does experience affect judgements of pain behaviour? Evidence from relatives of pain patients and healthcare providers. Pain Res. Manag. 6, 105–112 (2001). 47 Prkachin KM, Mass H, Mercer SR. Effects of
exposure on perception of pain expression. Pain 111, 8–12 (2004).
376
Pain Manage. (2011) 1(4)
48 Helson H. Adaptation-Level Theory.
Harper & Row, New York, NY, USA (1964). 49 Prkachin KM. Dissociating deliberate and
spontaneous expressions of pain. Pain 51, 57–65 (1992). 50 Kappesser J, Williams AC de C,
Prkachin KM. Testing two accounts of pain underestimation. Pain 124, 109–116 (2006).
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