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Pain assessment in elderly adults with dementia Thomas Hadjistavropoulos, Keela Herr, Kenneth M Prkachin, Kenneth D Craig, Stephen J Gibson, Albert Lukas, Jonathan H Smith Lancet Neurol 2014; 13: 1216–27 See Online for podcast Department of Psychology, University of Regina, Regina, SK, Canada (Prof T Hadjistavropoulos PhD); College of Nursing, University of Iowa, Iowa City, IA, USA (Prof K Herr PhD); Health Psychology Laboratory, University of Northern British Columbia, Prince George, BC, Canada (Prof K M Prkachin PhD); Department of Psychology, University of British Columbia, Vancouver, BC, Canada (Prof K D Craig PhD); National Ageing Research Institute, Melbourne, Australia (Prof S J Gibson, PhD); Geriatric Department, Malteser Krankenhaus Bonn/Rhein-Sieg, Bonn, Germany (A Lukas MD); Department of Neurology, University of Kentucky, Lexington, KY, USA (J H Smith MD) Correspondence to: Dr Jonathan H Smith, University of Kentucky, 740 S Limestone, L445, Lexington, KY 40536, USA [email protected]

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Chronic pain is highly prevalent in the ageing population. Individuals with neurological disorders such as dementia are susceptible patient groups in which pain is frequently under-recognised, underestimated, and undertreated. Results from neurophysiological and neuroimaging studies showing that elderly adults are particularly susceptible to the negative effects of pain are of additional concern. The inability to successfully communicate pain in severe dementia is a major barrier to effective treatment. The systematic study of facial expressions through a computerised system has identified core features that are highly specific to the experience of pain, with potential future effects on assessment practices in people with dementia. Various observational–behavioural pain assessment instruments have been reported to be both reliable and valid in individuals with dementia. These techniques need to be interpreted in the context of observer bias, contextual variables, and the overall state of the individual’s health and wellbeing.

Introduction Despite its limitations, self-report of pain is often deemed to be the gold standard in pain assessment. However, self-report might become compromised in neurological disorders, such as dementia, in which individuals often have little ability to communicate.1 With increasing severity of cognitive impairment, the ability to self-report pain diminishes, contributing to difficulties in recognising and controlling pain.2–4 That said, pain in dementia is not consistently reported to be undertreated. For example, the authors of a Swedish population-based study,5 who reported similar pain treatment in samples of individuals with or without dementia, acknowledged that their findings contradicted previous research and attributed these results to the possibility of increased awareness of the need for adequate pain management in dementia. In addition to the incapacity to communicate pain, inadequate pain assessment, biases including racial and ethnic disparities, and altered pain processing owing to the underlying neuropathology might limit access to appropriate treatment.6,7 In these susceptible populations, a systematic, evidence-based approach is needed to best address this fundamental aspect of patient care. The projected ageing of our population, combined with a parallel increase in the worldwide prevalence of dementia and stroke, make effective pain assessment in dementia of paramount importance. Chronic pain in people aged 85 years or older is common and has a prevalence of 40–79%.8 The estimated incidence of chronic pain in adults is 4·69 per 100 person-years, and is similar between individuals aged younger than 50 years and those older than 80 years.9 Therefore, healthcare providers should actively screen for pain in elderly adults, and recognise that treatment disparities exist in this patient population. Improved recognition and treatment of pain has implications for improvement of quality of life, and reduction of fall risk, agitation, depression, and anxiety in elderly people.10,11 The assessment of pain in non-verbal adults with neurological disease is clinically challenging and requires an understanding of the neurobiology of both pain experience and expression, along with knowledge of the available range of clinical assessment instruments. In

this Review we summarise the published work on the pain experience in people with dementia and describe the state of the art in pain assessment in this population, with primary emphasis on original studies published in the past 5 years. This Review provides the necessary background on the relevant topics and a clinical approach to this challenging and important scenario. We aim to highlight the usefulness of non-verbal cues (eg, facial expression) as a means of accessing the subjective pain experience of an individual, an approach that in many ways has advantages compared with self-report. We chose to focus on dementia in view of the abundance of published work pertaining to this population; however, the general principles might prove applicable to patients with other neurological disorders who are also at risk of inadequate pain management, such as those with poststroke aphasia.12

Pain processing in healthy ageing and dementia When considering the pain experience of elderly people, it is important to be aware of any age-related alterations in pain report and processing and factors that might contribute to such changes. Uncontrolled clinical studies reveal that pain might be a less frequent and severe presenting symptom in ageing people in various acute medical complaints, including pneumonia, appendicitis, myocardial ischaemia, postoperative pain, cancer, and peptic ulcer.13 Psychophysical studies of experimental pain provide some evidence for a slight increase in pain threshold (ie, implying a reduced sensitivity to mild pain) with advancing age, particularly for thermal pain stimuli.13 This finding has been supported by a metaanalysis of psychophysical studies.14 The results for other stimulus methods (ie, electrical, mechanical, and ischaemic) are more equivocal, with reports of no change or even decreased pain thresholds in older adults.15,16 Agerelated loss in the structure and function of the peripheral (mainly Aδ fibres)17 and CNS pathways implicated in the processing of noxious information have been noted,18,19 and reduced pain sensitivity is a likely consequence. Results from a functional neuroimaging study20 showed an age-dependent reduction in pain report and in the activation of middle insular cortex and primary www.thelancet.com/neurology Vol 13 December 2014

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somatosensory cortex in response to a 44°C heat stimulus. This finding contrasts with that of an earlier study21 using noxious mechanical stimulation, in which the only structure to show an age-related change in activation was the basal ganglia, thereby reinforcing the method-specific findings from previous psychophysical studies. Neurobiological and psychosocial changes in pain processing and interpretation might be expected to compromise the biological warning function of pain, lead to under-reporting of pain, and potentially place the older person at increased risk of undiagnosed disease or injury. However, modification in pain processing during later life is complex. Psychophysical studies of pain tolerance show the opposite direction of effect, with elderly adults being less able to endure strong pain sensations. Results from ten independent studies showed reduced pain tolerance as a function of age, irrespective of stimulus method (electrical, ischaemic, mechanical, heat, or cold).13,14 Studies of descending modulation from endogenous pain inhibitory systems reveal age-related impairment in opioid and non-opioid mechanisms in both animals and man.22–25 The magnitude of deterioration is large with elderly people showing less than a third strength of the induced endogenous inhibitory effects on pain sensitivity when compared with younger adults (generally younger than age 50). Another relevant consideration to explain decreased pain tolerance is the role of age differences in neuroplasticity. For example, temporal summation of noxious heat seems to occur more readily in the CNS of elderly people than in the CNS of young adults.15,16,26,27 In elderly adults, a long-lasting period of secondary hyperalgesia after an injury with topical capsaicin also shows a persistence of sensitisation and a much slower resolution of neuroplastic changes once they have occurred.28 In combination, these findings showed that as individuals age, they become more susceptible to strong pain in view of the decreased tolerance, endogenous inhibition, and persistence of sensation, once it has occurred. Dementia might exacerbate agerelated impairments in pain processing due to the additional burden of cognitive impairment and associated neurodegenerative loss in regions typically associated with higher levels of CNS processing of noxious information.13,29 People with Alzheimer’s disease have increased facial expressions of pain and enhanced withdrawal reflexes30,31 but their report of pain is decreased and their autonomic reactions in response to acute medical procedures, such as injection or venepuncture, are blunted.32 Pain threshold and tolerance increase in people with frontotemporal dementia,33 whereas pain threshold is unchanged in people with Alzheimer’s disease, although pain tolerance is increased, presumably owing to the topography of the underlying illness.34,35 A study36 from 2014 did not replicate these findings, with no reported change in pain tolerance to ice water and a decreased pain tolerance to mechanical pressure. www.thelancet.com/neurology Vol 13 December 2014

However, in patients with Alzheimer’s disease (figure 1), a study37 using fMRI revealed increased pain-related activations in the dorsolateral prefrontal cortex, midcingulate, and insula (regions involved in the cognitive and affective components of pain processing).38 To reconcile these different findings is difficult, but it seems probable that the severity of dementia might be of crucial importance because most experimental studies have been done in patients with mild disease, whereas clinical measures of pain are often taken from those with more advanced disease. Based on the available evidence, it seems that dementia diminishes pain perception at least in more severe cases; however, further longitudinal research with improved measures is needed to substantiate this view and to explore possibilities of accelerated pain perception across the spectrum of dementia.

Clinical pain assessment in dementia Self-report of pain should be attempted in all people with dementia because it is the most readily available means to assess the subjective experience of pain. However, selfreport has important limitations and is often unobtainable in advanced dementia, because of impaired cognitive, linguistic, and social skills.39,40 In these cases, behavioural–observational pain assessment instruments have led to important developments.41 Autonomic reactions, such as diaphoresis or increase of blood pressure, heart rate, and respiratory rate, can indicate the presence of acute pain; however, such measures are not as useful to identify persistent pain.31 Furthermore, evidence that these autonomic reactions are blunted in people with dementia has been reported.31,42

Observer bias in pain assessment To make a clinical pain assessment based on observation, inherent biases that might confound the assessment and potentially diminish the likelihood of satisfactory delivery of care need to be identified. Perceptual processes implicated in the recognition of pain have been the focus of investigations in which observers are shown non-verbal behaviour, with known degrees of pain expression, including facial displays, and infer the presence of pain or its intensity. Observer judgments are the product of both bottom-up input (ie, observation of self-report and nonverbal expression), and top-down processing, wherein observer knowledge, experience, and biases affect the judgments.43 Such studies show that observers are sensitive to pain expression when identifying its presence or the difference between broad categories of pain expression (no pain, mild pain, and strong pain).39 Indeed, children as young as 5 years of age discriminate the presence and severities of pain in others quite effectively.44 Neuroimaging studies45,46 in which observers are shown recordings of pain expression consistently show activation in some of the brain regions implicated in the processing of perceived pain, including the bilateral anterior insular cortex and the ventral and mid-dorsal anterior cingulate cortex. 1217

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patterns similar to those often seen in pain empathy studies, including in the anterior insula, somatosensory cortex, periaqueductal grey, and anterior cingulate cortex. By contrast, acupuncture physicians showed no change in insular or cingulate cortex activation patterns; rather, activation in the medial and superior prefrontal cortices and the temporoparietal junction was shown. The pattern of effects among those with expertise implicated activation of processes involved in emotion regulation and suggests a possible neurophysiological basis for the biases that have been shown in studies of the judgment of pain in others.

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Figure 1: Functional MRI of pain-related activity in Alzheimer’s disease Regions showing substantially greater pain-related activity in the Alzheimer’s disease patient group compared with healthy controls for the contrast between moderate pain and innocuous pressure. (A) Mid-anterior cingulate cortex, supplementary motor area, superior parietal lobule, and cerebellum. (B) Medial thalamus. (C) Bilateral primary motor cortex and ipsilateral dorsolateral prefrontal cortex. (D) Mid-anterior cingulate cortex, supplementary motor area, and premotor cortex. The images are shown in neurological convention with the left hemisphere on the left side of the image. Statistical maps are displayed on the average of all patients’ T1-weighted anatomical image, normalised into standard space. Figure adapted from Cole and colleagues, by permission of Oxford University Press.37

Nevertheless, observers display substantial biases in their investigation of pain in others. Studies have documented general bias, in which observers consistently underestimate pain in others.47 This judgment bias seems to vary with several factors, including the race of the person being assessed,48 their likability,49 and information about their motivations.50 Observers have been reported to be most sensitive or competent in pain estimation when observing facial expressions of pain in elderly people with dementia.39 The underestimation bias is enhanced among observers with clinical experience with pain sufferers,47 and experimental studies have shown that it can be produced by artificial overexposure to evidence of pain in others.51,52 This bias might show functional brain changes associated with the regulation of responses to pain in others. Cheng and colleagues53 compared fMRI activation patterns between naive observers and experienced acupuncture physicians as they observed animations of needle insertions. Naive observers showed activation 1218

Many self-report instruments are unidimensional, in that they provide an indicator of pain intensity alone, disregarding other pain qualities, location, and impact on function. These scales are generally reliable and valid in elderly adults who are able to provide a self-report.1 Indeed, several studies have lent support to the psychometric properties of these instruments in people with mild-to-moderate dementia, including reliability, criterion, and construct validity (eg, scores increase as a function of the extent that a situation or condition is believed to be painful).54 Moreover, research has shown that elderly patients with mild-to-moderate dementia are able to interpret such instruments correctly, although clinicians should be sensitive to deterioration of cognitive and linguistic capabilities.54–56 A widely used method is the Visual Analogue Scale (VAS), a 10 cm line with the extremes no pain (0) to worst possible pain (10). The VAS is one of the most frequently used assessment instruments in younger adults but has a substantially high error rate (almost 20%) among older adults compared with the Numeric Rating Scale (NRS) and the Verbal Descriptor Scale (VDS), thus it is not recommended in this population. The NRS comprises a line marked with numbers 0–10 at equal intervals, where 0 is no pain and 10 is worst pain imaginable. This scale is reliable and has been validated for use with elderly adults.57–59 Completion rate was high in people without cognitive impairment but substantially decreased for those with mild (75·5%) and moderate (57·5%) impairment.60 The VDS consists of verbal indicators ranging from no pain to excruciating pain.61 Results from several studies62 have shown that older adults often prefer the VDS when given a choice. Although language skills diminish with the course of the dementia, the ability to use words to express pain intensity might be still stable. Hence, up to 90% of people with moderate cognitive impairment were able to use the VDS accurately.60 Furthermore, even in severe dementia, there were still people capable of using a simplified version of this instrument.63 The Iowa Pain Thermometer (IPT) uses a combination of approaches, such as a vertical VDS adjacent to a graphic thermometer showing a colour gradation from white to red.64 The IPT has both a low rate www.thelancet.com/neurology Vol 13 December 2014

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of unscorable responses and is preferred by older adults with cognitive impairment.64 The Faces Pain Scale (FPS), initially developed for children,65 consists of a range of facial expressions arranged in hierarchical order. Both the FPS and the Faces Pain Scale-Revised (FPS-R) are reliable and valid in older adults with cognitive impairments from different racial backgrounds.64,66–69 That said, some caution should be exercised when using the FPS in view of the possibility that emotional facial recognition deficits,70 often seen in people with cognitive impairments, have the potential to interfere with use of the scale. This issue requires further investigation. In summary, self-report can be an accurate and reliable method for classification of pain1 that should be attempted in all patients and tends to be useful even in patients with mild-to-moderate dementia.1,60 The ability to comprehend methods such as the FPS should be assessed in patients with cognitive impairment. Clinically, assessment can be accomplished by asking the person to show on a selected instrument where they would place high and low ratings of pain. For those with severe dementia, assessment is more likely to be unobtainable, and use of an observational instrument would be strongly recommended, in addition to using information from other sources to measure the potential presence of pain (eg, medical history, physical examination, present painful conditions or procedures, and surrogate reporting).

Observational pain scales in dementia Over the past 15 years, there has been a surge in the development of specialised observational instruments designed to assess pain in patients with dementia.71–78 This work and resulting instruments have been summarised in several reviews and empirical instrument assessments.41,79 Systematic literature-based studies of existing assessment methods have compared up to 24 instruments.41,80,81 Despite the relatively large number of existing observational instruments for the assessment of older adults with dementia (panel 1), some methods have been rated consistently more highly than others in literature reviews and empirical investigations that include psychometric comparisons within a single patient sample.41,79–81,85,104 The instruments with consistently positive assessments include the Abbey Pain Scale (Abbey),77 the DOLOPLUS2,87,88 the Pain Assessment in Advanced Dementia (PAINAD),71 and the Pain Assessment Checklist for Seniors with Limited Ability to Communicate (PACSLAC).73 The Non-Communicative Patient’s Pain Assessment Instrument (NOPPAIN)72 has also been deemed to have strong features by the National Nursing Home Pain Collaborative.41 Across these reviews, there is still no one instrument that meets all purposes, and clinicians should consider the evidence and clinical usefulness of a recommended instrument for their specific population and setting. www.thelancet.com/neurology Vol 13 December 2014

Studies that advance our knowledge by examination of psychometric properties across scales and investigation of unique characteristics of instruments might make them stronger or weaker from a clinical standpoint.57,82,85,111 Some of this research85 has applied common sets of criteria (eg, examination of reliability coefficients, magnitude of effect in discrimination of painful from non-painful state). Obviously, recommendations from these studies only show the qualities of the specific instruments included in each analysis. Nonetheless, among the most important considerations for psychometric observational instrument comparisons would be inter-rater reliability (to ensure that different clinicians rating the same patient obtain similar results), sensitivity of the instrument to discriminate painful from non-painful states, and specificity (ie, ability to discriminate pain from other types of distress). To date, relevant research has indeed focused on reliability and sensitivity,57,81,85 and we cover such findings in this Review. Nonetheless, research on the specificity of the instruments is scarce.73 Some instruments, such as the MOBID-2, have had continued development, assessment, and use in clinical trials but have not been tested adequately outside the country of origin. Continuing research is focusing on the identification of specific behaviours that might identify pain in people with dementia,111 and on examination of the relation between scores on observational pain instruments and self-reported pain.57 Facial expression is important as a non-verbal pain behaviour and, in a comparative study111 of six methods, three (Abbey, PACSLAC, and PAINAD) were Panel 1: Instruments suitable for the assessment of pain in the elderly adult with dementia • • • • • • • • • • • • • • •

Abbey Pain Scale77,82–84 Checklist of Non-Verbal Pain Indicators (CNPI)78,84,85 Certified Nursing Assistant Pain Assessment Tool (CPAT)75,86 DOLOPLUS-287,88–90 Discomfort Scale in Dementia of the Alzheimer’s Type (DS-DAT/DS-DAT modified)91–95 EPCA-296 Mahoney Pain Scale97 Mobilization-Observation-Behaviour-Intensity-Dementia (MOBID and MOBID-2) Pain Scale74,98,99 Non-Communicative Patient’s Pain Assessment Instrument (NOPPAIN)57,72,85,100 Pain Assessment in the Communicatively Impaired (PACI)101–103 Pain Assessment Checklist for Seniors with Limited Ability to Communicate (PACLSAC and PACSLAC-II)2,73,85,104–107 Pain Assessment for the Dementing Elderly (PADE)85,108 Pain Assessment in Advanced Dementia (PAINAD)57,71,82,85,109 Pain Assessment in Noncommunicative Elderly Persons (PAINE)76 The Rotterdam Elderly Pain Observation Scale (REPOS)110

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noted as most promising to capture relevant facial expressions. In addition to noting changes in facial expression, behavioural signs in other domains (eg, vocalisations and body movements) have also been incorporated into different observational pain scales (panel 2). In a related study, Lukas and colleagues57 reported correlations between self-reported pain and scores on the Abbey, PAINAD, and NOPPAIN, whereas Kaasalainen and colleagues2 identified similar correlations between self-reported pain and PACSLAC scores. Despite these advances some limits to our knowledge about instrument use for non-verbal pain behaviour assessment are noted. These restrictions include insufficient standardisation of administration conditions (eg, duration of administration and the type and source of pain being reported could affect scores), insufficient research on the effects of pain fluctuation on scores, insufficient normative information Panel 2: Pain behaviours used in validated observational pain scales Facial expressions • Grimacing, tighter face, wrinkled nose • Brow lowering, closed or tightened eyes, upper lip or cheek raising • Wincing • Squinting or narrowing of eyes • Mouth opening Vocalisations • Moaning, groaning, grunting, crying • Specifc sounds or words for pain (eg, ”ow”, ”ouch”, and ”that hurts”) • Gasping or noisy breathing Body movements • Flinching or pulling away • Thrashing, rocking • Refusing to move, moving slow • Bracing, avoidance of certain body positions • Rubbing, holding, and/or guarding sore area • Limping • Clenched fist • Going into fetal position, knees pulled up • Stiff or rigid • Shaking or trembling Changes in interpersonal interactions • Not wanting to be touched, not allowing people near • Decreased social interactions and communication • Difficult to console or reassure Changes in activity patterns or routines • Sleep changes • Sudden cessation of common routines, decreased activity Mental status changes • Are there mental status changes that could be due to pain, and cannot be attributable to another cause (eg, delirium due to medication)? Modified with permission from the AGS Panel on Persistent Pain in Older Persons.112 We derived the list of validated pain behaviours from well established observational pain scales (PAINAD,71 NOPPAIN,72 PACSLAC-II,113 and DOLOPLUS2114), and from studies using FACS.87 Pain behaviours are most reliably assessed with a complete validated pain instrument.

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to help interpretation of scores, difficulty to establish severity of pain from behavioural assessment, and overlap of behavioural indicators representing different conditions (eg, pain and delirium). As such, further research is warranted. Additionally, more comparative studies to help identify the instruments most effective in detection of pain and most sensitive in detection of response to treatment are needed to guide instrument refinement and bestpractice recommendations. The following is a brief overview of selected instruments that have received the most support across recent reviews and published work:

Abbey Pain Scale The Abbey scale contains six items (facial expression, change in body language, vocalisation, behavioural change, physiological change, and physical change).77 The instrument has satisfactory internal consistency and differentiates non-painful from painful situations.85 Concurrent validity has also been established.57 The scale was endorsed by the Australian Pain Society and was deemed to be one of three instruments with the strongest support in a systematic comparison of 24 instruments to use for elderly people with dementia.80

DOLOPLUS 2 This instrument was originally developed in French but has been translated into English and has been used in English speaking settings. DOLOPLUS 2 consists of two psychomotor (washing and dressing; mobility), five somatic (protection of sore areas, sleep pattern, somatic complaints, protective body postures adopted at rest, and expression), and three psychological (problem behaviour, social life, and communication) items. The DOLOPLUS 2 has satisfactory internal consistency81 and leads to reliable measurement.21 Moreover, scores differ between groups of patients believed to have pain and patients who were deemed pain-free.104 DOLOPLUS 2 was deemed to be one of several methods with high psychometric support in two systematic comparisons of instruments.80, 81

NOPPAIN This method is based on the observation of six pain behaviours (facial expressions, pain-related words, rubbing, bracing, pain noises, and restlessness) during common care tasks, such as bathing and dressing. Good inter-rater agreement and ability to differentiate painful from non-painful states have been shown.57,72,100 The National Nursing Home Pain Collaborative41 recognised the strengths of this tool with a focus on key pain behaviours but concluded that clinical use might be limited by the complex structure of the NOPPAIN.

PAINAD The PAINAD is a brief instrument that includes five items (breathing, negative vocalisations, facial expression, body language, and consolability). PAINAD has moderate www.thelancet.com/neurology Vol 13 December 2014

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internal consistency and concurrent validity.71,85,109 PAINAD scores decrease after administration of analgesics8 and vary as a function of potentially painful activity.85,104 The National Nursing Home Pain Collaborative41 recommended the PAINAD as a clinically useful instrument.

PACSLAC and the PACSLAC-II The PACSLAC consists of 60 items (eg, grimacing, limping, or not wanting to be touched), which are rated as present or absent, and is the only published instrument of its kind that incorporates comprehensive coverage of all observational assessment domains deemed important by the American Geriatrics Society guideline.115,116 PACSLAC has good internal consistency, inter-rater, and test–retest reliability. In several studies, the PACSLAC has discriminated pain from non-pain-related states.73,85,104 Similar to the PAINAD, the PACSLAC was recommended as one of the best clinically useful instruments80 and one of the psychometrically strongest instruments.80,81 In a comparison of key instruments, Lints-Martindale and colleagues85 concluded that, although most instruments had satisfactory psychometric properties, the PACSLAC accounted for variance in the discrimination between painful and non-painful states over and above that of all of the other instruments combined. The PACSLAC was revised and shortened (31 items) with removal of items that could potentially be confused with signs of delirium. The PACSLAC-II113 retained coverage of American Geriatrics Society (AGS)116,117 recommended domains and has good reliability and ability to discriminate pain from non-pain-related states. In a comparison similar to that of Lints-Martindale and colleagues,85 Chan and colleagues113 concluded that the ability of the PACSLAC-II to discriminate between painful and non-painful states was better than that of seven other instruments under investigation (including the PACSLAC).

Translations in languages other than English Many of the observational instruments for elderly adults with dementia, including PAINAD,83,118–120 PACSLAC,2,105,121,122 and DOLOPLUS2,87,88,104,123 have been translated into other languages, although the psychometric properties of some translated versions have not been adequately investigated in the new language. Considerable work is needed to research translation and establish psychometrics in other additional languages and cultures.

Consensus recommendations and guidelines for pain assessment in elderly adults with dementia Several influential organisations and other expert groups have published guidelines pertinent to the pain assessment of the elderly adult with dementia. Some of these documents are focused on both pain assessment and management,116,117,124–126 whereas others focused only on assessment.1,41,127 Some guidelines focused on elderly www.thelancet.com/neurology Vol 13 December 2014

people with and without dementia,1,116,117,127 others only on people with dementia,41,125,128 and others on various populations with little ability to communicate, including people with dementia.126 Moreover, some guidelines recommend specific self-report instruments125 and specific observational instruments41,125 for the assessment process (panel 3). In view of the restricted ability to communicate in people with dementia, it should be noted that the AGS116 has identified domains of non-verbal pain behaviour that should be considered: facial expressions, verbalisations and vocalisations, body movements, changes in interpersonal interactions, changes in activity patterns or routines, and mental status changes. Although coverage of these domains can be used to assess the comprehensiveness of observational pain assessment approaches, ongoing research is focused on identifying the key behaviours that are most useful to assess the presence and severity of pain and to establish the best combination of behaviours85,111 and methods to assess pain in people with dementia.111 Although differences are noted in recommendations regarding specific instruments, there is no evidence of disagreement across guidelines when it comes to general principles of assessment (figure 2). In general, there is recognition of seven criteria (panel 4). Experts in the specialty generally agree that self-report of pain intensity often can be obtained effectively with simple unidimensional scales such as the NRS and the VDS in patients with mild-to-moderate dementia.1,55,125,127 However, clinicians should be aware that valid pain assessment in non-verbal patients is still possible with other approaches. When it comes to recommendations for use of specific observational pain assessment instruments, different guidelines41,125 have recommended different instruments, which often relate to the country of origin of the guideline. Since development and assessment of such instruments has progressed rapidly in the past years, discrepant recommendations about specific instruments can be explained, partly, as a function of

Panel 3: Key guidelines of pain assessment in the patient with dementia • International Interdisciplinary Consensus Statement on Pain Assessment in Older Persons1 • National Nursing Home Pain Collaborative41 • American Geriatrics Society (AGS)116,117 • American Medical Directors’ Association (AMDA) Pain Management Guideline124 • Pain in residential aged care facilities (Australian Pain Society)125 • Task force of the American Society for Pain Management Nursing (ASPMN)126 • The British National Guideline for Assessment of Pain in Older People127 • Transforming pain management in long-term care pain management in North America128 • Australian and New Zealand Society for Geriatric Medicine129 • Multidisciplinary guideline (Dutch)130

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those described in this Review), an update of the guidelines on specific observational instruments is clearly needed.

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Figure 2: Components of pain assessment in non-verbal adults Pain assessment in non-verbal adults necessitates the use of behavioural recordings, which should be interpreted with regard to contextual variables and in light of the individual’s general state of health and wellbeing.

Panel 4: A Clinical approach to pain assessment of the patient with dementia • Pain has many dimensions and a thorough assessment should not be limited to pain intensity. Instead, functional status, emotional functioning, and situational and contextual factors should also be assessed. Moreover, pain assessment information should be integrated with the results of physical examinations, medical test findings etc.1,41,116,117,125–128 • Self-report should be attempted with all patients1,41,116,117,125–128 since patients with mild-to-moderate and, sometimes, severe dementia can often provide valid self-reports of pain.57 Adaptations should be made to match the capabilities of the individual (eg, use of simplified language and large fonts).1,41,116,117,125–127 • Validated standardised observational approaches80, 81 should be used to decrease the risk of observer bias, especially for patients with little ability to communicate verbally.1,41,116,117,125–128 • Caregiver and other collaborative informant reports should be solicited and can contribute to the assessment process,1,41,116,117,125–128 although concern with accuracy of proxy reports has been noted.131 • Pain assessment during movement is more likely to elicit pain behaviours than pain assessment during rest.1,41,116,117,125–128 • An individualised approach to assessment, whereby pain is assessed on a regular basis and fluctuation from a patient’s normal pattern of scores is recorded, should be pursued.1,41,116,125–128 • Assessment of pain before and after the administration of a pain management intervention is useful.1,41,116,117,126,128

For the European Cooperation in Science and Technology see http://www.cost-td1005.net

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when the guideline was prepared (eg, the Australian Pain Society guideline was prepared in 2005, whereas the National Nursing Home Collaborative guideline was prepared in 2011 after substantial progress in the discipline was made). In view of advances (including

Conclusions and future directions Individuals with dementia are at high risk for underrecognition, underestimation, and undertreatment of pain, despite pain continuing to be highly prevalent with ageing. Restrictions in the communication of pain are a crucial barrier in dementia, because self-report of pain is deemed to be the most readily available way to access the subjective pain experience, despite its shortcomings. Consequently, systematic assessment of non-verbal expressions is of great importance in the clinical pain assessment of patients with dementia. In view of the great deal of information that can be communicated through facial expression of pain, we have incorporated an in-depth examination of this topic in panel 5. Training in the recognition of empirically described facial expressions of pain will lead to more reliable and accurate judgements. Nevertheless, fine grained analysis of facial expressions might prove difficult for clinical settings until advanced, automated, and affordable computer vision technologies, capable of unobtrusively detecting facial expressions of pain, could become a reality. Until such time, clinically useful pain assessment methods for patients with dementia have been developed. These methods can be incorporated into practice to improve identification of pain in people with dementia. Further refinement and testing of the plethora of instruments that has emerged is needed, including accounting for effects of comorbidity on pain expression (eg, hypomimia and facial paresis). In figure 2, we present a model of pain assessment that incorporates the central key elements from authoritative guideline documents (see panel 3). To summarise, good pain assessment of patients with dementia and serious restrictions in ability to communicate should incorporate a thorough history, proxy reports, results of physical examinations and medical tests, assessment of functional status, consideration of situational and contextual variables, assessment of emotional status, self-reported pain (if available), and observational pain assessment. In turn, solid observational pain assessment should incorporate use of a standardised, well validated instrument, repeated results over time (under consistent circumstances), observation during movement, and pain assessment before and after pain management (eg, analgesic trial). In panel 2 we have summarised key pain behaviours used in validated observational assessment instruments. Continuing research also includes efforts by the European Cooperation in Science and Technology to develop a consensus pain instrument to be used in individuals with dementia. Further research should www.thelancet.com/neurology Vol 13 December 2014

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attempt to validate these scales in other susceptible patient populations with neurological disease. Additionally, continued development of real-time,

automated video assessments of facial pain expression might prove invaluable in view of the present absence of clinically validated pain biomarkers.

Panel 5: Facial expression of pain Although pain is often construed as private and subjective, non-verbal overt behaviour typically can be seen to change systematically with the experience of pain. A range of behavioural signs that might be associated with pain, such as facial expressions and mental status changes, has been studied (panel 2). Some behaviours, such as withdrawal or guarding, are recruited to diminish either the threat from the source of pain or to manage the pain itself. Other behaviours serve a primary communicative function, to send a signal that pain is being experienced.132 Changes in facial expression fall within this category and they seem to represent the most sensitive and specific non-verbal manifestations of pain. As the principal object of social attention, the face plays a central part in regulation of social interactions in both human and non-human species.133 Dynamic changes in facial appearance are well established to communicate a broad range of involuntary and intentional cognitive and affective states, including pain. According to an established understanding of the regulation of facial expression,134 upper and lower motor neuron pathways subserve a distinction between volitional control and spontaneous emotional expression. A cortical pyramidal motor tract controls voluntary facial expressions and a subcortical extrapyramidal tract drives spontaneous expressions of felt emotions. The pyramidal system enables human beings to simulate facial expressions of emotions not actually experienced or to suppress and exaggerate their appearance, and seems to be more important to learned or skilled variations in facial expression.The pyramidal system is more closely associated with the neural tracts that permit the highly skilled, unilateral movement of the lower face. By contrast, the phylogenetically older extrapyramidal motor system seems driven more by emotional centres of the brain; hence, it is associated with genuinely felt emotions, and is less associated with voluntary control and awareness of the facial expression. The complexities have not been fully worked out because reflexive systems are subject to some voluntary control. People are able to suppress reflexes in general, including facial actions, although not wholly, and they can exaggerate the display.135–137 The traditional account of neural regulation of facial expression has been supplemented by studies of pain expression that benefit from functional imaging. Kunz and colleagues138 measured blood-oxygenation level dependent (BOLD) functional MRI responses to thermal pain in relation to pain expression. Participants who showed vigorous facial pain expressions showed increased BOLD activity in motor structures, including the face region of the primary motor cortex bilaterally and the supplementary motor area. For these particularly expressive subjects, activation was also seen bilaterally in the primary sensory cortex (S1) and the posterior insula. By contrast,

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participants who were facially inexpressive showed increased activity in medial prefrontal cortex, the middle frontal gyrus and in the caudate nucleus, suggesting that prefrontal and caudate structures are involved in suppression of pain expression. The facial changes that occur during pain have been the subject of intense study since the development of the Facial Action Coding System (FACS).139 FACS is a fine-grained, objective, anatomically-based coding system that categorises facial expressions using a comprehensive set of 46 operational definitions of specific actions (Action Units). The functional neuroanatomical movements identified are necessary and sufficient to code any facial expression. FACS has been applied in many studies of experimental and clinical pain, to encompass the lifespan from neonates to older adults, and in people with dementia.111,140–142 Although some variation has been reported, there is substantial agreement across studies that a small subset of facial actions increases in likelihood, frequency, intensity, and duration when people experience pain. Actions of the corrugator, orbicularis oculi, and levator muscles produce brow lowering, orbit tightening, eyelid closure and upper lip raising, respectively.140,143,144 The combination of these muscle activities is often accompanied by opening of the mouth as well. Other actions, such as those produced by zygomatic and risorius muscles also correlate with pain in some studies; psychometric analyses show, however, that these comprise a different reaction.144 The consistency with which these facial movements appear with pain produced by different modalities, and in different populations,141 suggests that brow lowering, orbit tightening, upper lip raising, and eyelid closure constitute a unitary, core set of facial movements during pain. Studies of pain during human ageing with FACS have shown that the pain expression is still consistent, even in patients with mild cognitive impairment.42,140, 142 Dementia, however, is associated with enhanced pain expression, possibly as the result of diminished inhibitory controls.42 Therefore, the application of FACS to pain assessment represents a major advancement with future implications for instrument development and refinement. Standard practice for the measurement of pain expression to date has been based on manual scoring of the presence and intensity of facial actions, but fully automated computer vision systems are emerging that continuously analyse facial movements from video in real time with dimensions corresponding to the FACS Action Units.137, 145–147 This new technology might have future clinical application for real-time objective pain assessment, particularly in terms of capturing spontaneous, ongoing pain, thereby reducing clinician time commitments and the potential for clinician bias.

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Search strategy and selection criteria We identified references for this Review through Medline from Jan 1, 1980 to Oct 1, 2014, and review of references cited by relevant articles. Search terms included “pain assessment” and “older adult”, “elderly”, “cognitive impairment”, “dementia”, “limited ability to communicate”, and “nonverbal”. We then established selected articles on the basis of topical relevance and effect. Although inherent bias is always present in selected studies to be published in any review,148 emphasis was put on work published in the past 5 years, we hope to have minimised this bias.

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18 Contributors All authors contributed to the literature search, drafting of the manuscript, and approval of the final version. Declaration of interests TH declares that, although he does not have a financial interest in the PACSLAC/PACSLAC-II, he is one of the developers of the PACSLAC/ PACSLAC-II, an instrument that is being considered, along with others, in this Review. SJG receives payments from CSL Pty and Pfizer for participation on advisory boards. SJG declares no competing interests related to the content of the proposed Review. AL receives support from Mundipharma GmbH (partly beside the Robert Bosch Foundation) a present research project, validation of the German PAINAD, a doubleblind randomised trial aimed to investigate the validity of the PAINAD scale in people with severe dementia, unable to give oral response; additionally, AL has received renumeration in the course of giving individual lectures at Mundipharma GmbH and Pfizer GmbH during the past 5 years. JHS, KH, KMP, and KDC declare no competing interests. References 1 Hadjistavropoulos T, Herr K, Turk DC, et al. An interdisciplinary expert consensus statement on assessment of pain in older persons. Clin J Pain 2007; 23 (suppl 1): S1–43. 2 Kaasalainen S, Akhtar-Danesh N, Hadjistavropoulos T, Zwakhalen S, Verreault R. A comparison between behavioral and verbal report pain assessment tools for use with residents in long term care. Pain Manag Nurs 2013; 14: e106–14. 3 Markey G, Rabbani W, Kelly P. 022: association of dementia with delayed ED analgesia in patients over 70 with acute musculoskeletal injury. Emerg Med J 2013; 30: 875. 4 McDermott JH, Nichols DR, Lovell ME. A case-control study examining inconsistencies in pain management following fractured neck of femur: an inferior analgesia for the cognitively impaired. Emerg Med J 2013; 31: e2–8. 5 Haasum Y, Fastbom J, Fratiglioni L, Kareholt I, Johnell K. Pain treatment in elderly persons with and without dementia: a population-based study of institutionalized and home-dwelling elderly. Drugs Aging 2011; 28: 283–93. 6 Sengupta M, Bercovitz A, Harris-Kojetin LD. Prevalence and management of pain, by race and dementia among nursing home residents: United States, 2004. NCHS data brief 2010; 1–8. 7 Tait RC, Chibnall JT. Racial/ethnic disparities in the assessment and treatment of pain: psychosocial perspectives. Am Psychol 2014; 69: 131–41. 8 Helme RD, Gibson SJ. The epidemiology of pain in elderly people. Clin Geriatr Med 2001; 17: 417–31. 9 Shi Y, Hooten WM, Roberts RO, Warner DO. Modifiable risk factors for incidence of pain in older adults. Pain 2010; 151: 366–71. 10 Hellstrom Y, Persson G, Hallberg IR. Quality of life and symptoms among older people living at home. J Adv Nurs 2004; 48: 584–93. 11 Smalbrugge M, Jongenelis LK, Pot AM, Beekman AT, Eefsting JA. Pain among nursing home patients in the Netherlands: prevalence, course, clinical correlates, recognition and analgesic treatment—an observational cohort study. BMC Geriatr 2007; 7: 3. 12 Smith JH, Bottemiller KL, Flemming KD, Michael Cutrer F, Strand EA. Inability to self-report pain after a stroke: a population-based study. Pain 2013; 154: 1281–86.

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