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The facial expression of pain in patients with dementia
Pain 133 (2007) 221–228 www.elsevier.com/locate/pain
The facial expression of pain in patients with dementia Miriam Kunz a,b,*, Siegfried Scharmann b, Uli Hemmeter b, Karsten Schepelmann c, Stefan Lautenbacher a b
a Physiological Psychology, Otto-Friedrich University Bamberg, Germany Department of Psychiatry and Psychotherapy, Philipps University Marburg, Germany c Department of Neurology, Philipps University Marburg, Germany
Received 26 April 2007; received in revised form 21 August 2007; accepted 10 September 2007
Abstract The facial expression of pain has emerged as an important pain indicator in demented patients, who have difficulties in providing self-report ratings. In a few clinical studies an increase of facial responses to pain was observed in demented patients compared to healthy controls. However, it had to be shown that this increase can be verified when using experimental methods, which also allows for testing whether the facial responses in demented patients are still typical for pain. We investigated facial responses in 42 demented patients and 54 aged-matched healthy controls to mechanically induced pain of various intensities. The face of the subject was videotaped during pressure stimulation and was later analysed using the Facial Action Coding System. Besides facial responses we also assessed self-report ratings. Comparable to previous findings, we found that facial responses to noxious stimulation were significantly increased in demented patients compared to healthy controls. This increase was mainly due to an increase of pain-indicative facial responses in demented patients. Moreover, facial responses were closely related to the intensity of stimulation, especially in demented patients. Regarding self-report ratings, we found no significant group differences; however, the capacity to provide these self-report ratings was diminished in demented patients. The preserved pain typicalness of facial responses to noxious stimulation suggests that pain is reflected as validly in the facial responses of demented patients as it is in healthy individuals. Therefore, the facial expression of pain has the potential to serve as an alternative pain assessment tool in demented patients, even in patients who are verbally compromised. Ó 2007 International Association for the Study of Pain. Published by Elsevier B.V. All rights reserved. Keywords: Dementia; Pain; Facial expression of pain; Non-verbal communication
1. Introduction It is well known that the capacity to report pain is diminished in demented patients and that especially patients with moderate to severe dementia have difficulties to provide self-report ratings of pain (for comprehensive reviews, see [16,17,31]). Based on these findings, many authors have stressed the urgent need for alternative non-verbal pain-assessment tools in order * Corresponding author. Address. Physiological Psychology, University of Bamberg, Markuspl. 3, 96045 Bamberg, Germany. Tel.: +49 951 8631850; fax: +49 951 8631976. E-mail address: [email protected] (M. Kunz).
to rule out the possibility of an under-detection of pain in this patient group (for comprehensive reviews, see [17,18,32]). Amongst others, the facial expression of pain has been suggested as a possible non-verbal alternative to self-report ratings [14,20]. The facial expression of pain is considered to be one of the most prominent non-verbal pain behaviors because of its reflexive nature, its salience and because it can be distinctively differentiated from other affective states [4]. So far, there are only four studies which focused on facial responses to potentially noxious procedures in elderly individuals with dementia [11–13,27]. Facial responses during flu injections [11], venipuncture [12,27] and exacerbation of chronic musculoskeletal
0304-3959/$32.00 Ó 2007 International Association for the Study of Pain. Published by Elsevier B.V. All rights reserved. doi:10.1016/j.pain.2007.09.007
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pain during physical exercise [13] were videotaped and later analyzed using the Facial Action Coding System [5]. Although the studies differed immensely with regard to the way in which pain was induced or varied, the findings are surprisingly homogeneous. First of all, it was consistently found that facial responses to potential noxious procedures intensify (compared to a baseline period) and can be assessed even in demented patients, who are verbally compromised [11–13,27]. Furthermore, it was reported that facial responses in demented patients are augmented compared to responses in cognitively unimpaired controls [13,27]. However, the authors also presumed that this augmentation of facial responses in demented patients was mainly due to a rather unspecific overall increase of facial responses [11,12,27]. This impression, though, was not based on a systematic analysis aiming at differentiating between pain-relevant and pain-irrelevant facial responses. Therefore, the question remains on how pain typical are facial responses to noxious stimulation in demented patients. Is dementia really associated with an augmentation of facial responses during pain which is part of a general disinhibition of facial responses? Moreover, no study before applied experimental pain stimuli – in order to exert exact control over the noxious input – when analyzing facial responses in demented patients. Our aim was to investigate facial responses of patients with dementia by testing three hypotheses experimentally: (I) Demented patients show more frequent and intense facial responses during potentially noxious stimulation than healthy individuals. (II) This relative increase is due to an unspecific overall increase of facial responses in demented patients. (III) Facial responses of demented patients encode the intensity of potentially noxious stimulation less well than facial responses of healthy individuals do.
2. Materials and methods 2.1. Subjects Forty-two patients with dementia (mean age 76.7 ± 7.3 years; $:22, #:20) and 54 healthy control subjects (mean age 74.2 ± 5.6 years; $:43, #:11) over the age of 65 participated in this study. Control subjects were recruited amongst students of the Senior University at the University of Marburg. Patients with dementia were recruited amongst inpatients from the Department of Neurology and the Department of Psychiatry and Psychotherapy of the University of Marburg. None had taken any analgesic medication for at least 24 h prior to the test session. Participants with any condition – other than dementia in the case of the patients – that could affect pain perception and pain report such as diabetes, hypertension, periph-
eral and central neuropathy, neurological and psychiatric disorders were excluded from the study. Prior to the experiment, a thorough neurological examination (including examination of the sensory system, testing of deep tendon reflexes, autonomic testing, sural neurography, etc.) was conducted in order to identify persons who met the exclusion criteria. Moreover, a neuropsychological examination was conducted to evaluate the cognitive status of the subjects. Amongst others, the Mini Mental State Examination test (MMSE), according to Folstein et al. [8], was used to assess the cognitive status. Patients with dementia had a mean MMSE-score of 16.3 (±5.5SD) and healthy controls had a mean score of 29.5 (±0.8SD). Furthermore, patients with putative dementia were examined by a neurologist or psychiatrist and diagnosed according to the criteria specified by the ICD-10, NINCDS-ADRDA [24] and NINDS-AIREN [30]. According to these diagnostic guidelines, analyses of cerebrospinal fluid, blood chemistry analysis, EEG, CT or MRT and ECG analyses were conducted besides clinical assessment. 16 patients met the NINCDSADRDA criteria for the clinical diagnosis of probable Alzheimer’s disease (AD), 17 patients met the NINDS-AIREN criteria for the clinical diagnosis of probable Vascular Dementia (VD) and 9 patients were diagnosed as suffering from Mixed Dementia (MD).1 The study protocol was approved by the ethics committee of the medical faculty of the University of Marburg. We took care that only patients with dementia were included in the study who still had legal capacity. After being informed in a slow and simple fashion, which was adjusted to the individual intellectual capacities, subjects gave written informed consent. We also provided instructions during testing as simple as possible and monitored the patients continuously for any signs of undue discomfort (verbally or non-verbally), in which case we stopped testing immediately. Healthy subjects were paid for participation. 2.2. Materials and procedure All testing were conducted during the hours of 3.00–6.30 p.m. and lasted for approximately 2 h. The testing procedure included an examination of potential exclusion criteria and neuropsychological examination (approximately 1 h), the experimental pain test (20 min), a short break (10 min) and an assessment of autonomic and motor reflexes (30 min, the results of which are not reported here). All subjects were seated in an armchair after the physical examination. Experimental pain was induced by using pressure stimuli. A Fischer algometer (a force gauge fitted by a rubber disk with a surface of 1 cm2) was used to apply noxious mechanical pressure [7]. The algometer was slightly modified so that each stimulus onset could be electronically recorded and could be used as a trigger signal for the video analysis. In order to familiarize subjects with pressure stimulation, three stimuli of 2 to 3 kg (‘‘kg’’ is used as physical unit in the present study because the Fischer algometer is scaled like that) were applied to the thigh before tests started. In the test 20 stimuli varying between 1 and 5 kg (4 stimuli at each inten-
1
Other forms of dementia were deliberately excluded.
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sity) were applied to the right and left forearm in a random order, which had been determined once and was used for all subjects. Pressure was increased steadily at an application rate of 1 kg per second until maximum stimulus intensity was reached and then continued at that level for another 5 s. Since maximum stimulus intensities varied between 1 and 5 kg, it took between 1 and 5 s to reach maximum intensity. The interval between stimulus applications varied between 20 and 30 s. Pressure application was always performed by the same experimenter, who had been trained in using the Fischer algometer. 2.3. Self-report Right after each stimulus application, subjects were asked to give self-report ratings regarding the peak sensation felt. Self-report was assessed via a 6-point verbal category scale (no pain – mild pain – moderate pain – strong pain – very strong pain – extremely strong pain). 2.4. Facial expression of pain The face of the subject was videotaped throughout the entire session. The camera was placed in front of the subject at a distance of approximately 4 m. Before applying a stimulus, subjects were always instructed to focus on an emotionally neutral picture being positioned behind the camera in order to ensure a frontal view of the face. Subjects were also instructed not to talk during pain induction. To mark the onset of pain stimulation on the videotape (for further analysis), we switched on a signal light concurrently. The light was visible to the camera but not to the subject. The Facial Action Coding System (FACS) [5] was used to analyze facial responses. The FACS is based on anatomical analysis of facial muscle movements and distinguishes 44 different action units (AUs). These are the minimal numbered units of facial activity that are anatomically separate and visually distinguishable. The intensity for each action unit was rated on a 5-point scale (A–E) with A being the least intense of the action and E the maximum strength of the action. A FACS coder (qualified by passing an examination given by the developers of the system) identified the frequency of all 44 AUs and the intensity of 42 AUs (AUs 45 and 46 do not allow for intensity coding). A special software designed for analysis of observational data (the Observer Video-Pro (Noldus Information Technology)) was used to segment the videos and to enter the FACS codes into a time-related data-base. Time segments of 5 s beginning just after stimulus and had reached maximum were selected for scoring. In total, 20 segments of pressure stimulation (4 series of pressure stimuli from 1 to 5 kg) were analyzed. For purpose of necessary data reduction, we combined those AUs that represent facial movements of the same muscle as has been done in preceding studies without any loss of information (e.g. [15,19,28]). Therefore, AUs 1 and 2, AUs 6 and 7, AUs 9 and 10 as well as AUs 25, 26 and 27 were combined to form new variables. To select those AUs that were pain-relevant in the present experimental context and to summarize these facial responses by computing a pain-relevant composite score, several steps were necessary.
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(1) As has been done in earlier studies (e.g. [3,10,13,19]), we denominated only those AUs as pain-relevant that occurred in at least 5% of the pain segments2 recorded. We did this separately for demented patients and healthy controls (the results are listed in Table 1)3. (2) To determine which of these AUs listed in Table 1 were critically more frequent during pain segments than during non-painful segments, we computed effect sizes (Cohen’s d for two dependant groups) for these differences. Effect sizes were computed separately for the demented patients and healthy controls. The values of these effect sizes are also listed in Table 1. For further analysis only those Action Units which reached an effect size d P 0.5 (medium effect) in both groups (these AUs are shaded in grey in Table 1) were used to form a composite score of pain-relevant facial responses. (3a) Prior to computing the composite score, the frequency values of all Action Units had to be given weights. This was necessary because the frequency of AU 45 (blinking of the eye) is disproportionally higher than those of the other AUs. In order to reduce this numerical distortion, we decided to compute weighted frequency values for all AUs. This was done by dividing the frequency of each AU at each stimulus intensity by the mean frequency of the given AU across all stimulus intensities. (3b) Composite scores of pain-relevant facial responses were formed by calculating mean scores of those AUs that proved to be pain-relevant (shaded in grey in Table 1) separately for each stimulus intensity and separately for FACS frequency and FACS intensity. (3c) We also computed composite scores of pain-irrelevant AUs by calculating mean scores of all AUs that did not prove to be pain-relevant. This was done to allow for the comparison between pain-relevant AUs and pain-irrelevant AUs, and thus evaluate the ‘‘pain typicalness’’ of facial responses. 2.5. Statistical analysis 2.5.1. Group differences in facial responses to pain To evaluate the impact of dementia on facial responses to pain, we computed a multiple (for frequency and intensity values) analyses of variance with repeated measurements on two within-subject factors ‘‘stimulus intensity’’(1 to 5 kg) and ‘‘type of facial response’’(pain-relevant and pain-irrelevant AUs) as well as with one between-subject factor ‘‘group’’(demented patients and healthy controls). In case of significant group difference, t-tests were computed for single comparisons. 2.5.2. Group differences in self-report To evaluate the influence of dementia on self-report ratings, we computed analyses of variance with repeated measurements on one within-subject factor ‘‘stimulus intensity’’ (1 to 5 kg) and with one between-subject factor ‘‘group’’(demented patients and healthy controls). 2
All trials being rated as ‘‘mild pain’’ or more on the verbal scale were considered to be pain segments. Trials rated as ‘‘no pain’’ were considered to be non-painful segments. 3 The selection of AUs in this step was based on these subjects, who were able to report pain by ratings (see Results for details).
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Table 1 Facial action units (AUs) with a critical occurrence of more than 5% in denominated ‘‘pain’’-segments in healthy controls and in demented patients (see text for further explanations)
a b
Percent denotes the percentage of occurrence in the entire pain segments. Blinking of the eye can appear more than once in a time-segment of 5 s. Relative frequency of occurrence and effect sizes for frequency differences between ‘‘pain’’ and ‘‘non-pain’’ segments are given. Medium and strong effect sizes (e P 0.5) are marked in bold; AUs shaded in grey represent AUs that were consistently more frequent (e P 0.5) during pain segments in both groups.
Furthermore, we were also interested in evaluating the extent to which dementia interferes with the capacity to provide self-report ratings. Therefore, we computed for each subject the percentage of stimuli that the subject responded to with valid self-report ratings4 and correlated these values with the degree of cognitive impairment (MMSE-score). Findings were always considered to be statistically significant at a < 0.05.
3. Results 3.1. Influence of dementia on facial responses to pain Dementia had a significant main effect on the frequency and intensity of facial responses to pressure stimulation (see Table 2). As can be seen in Fig. 1, the frequency and intensity of facial responses were markedly increased in demented patients. Single comparisons (T-tests) revealed that group differences were most evident for pain-relevant AUs (significant results are displayed in Fig. 1). Accordingly, hypothesis I about the effect of dementia on the frequency and intensity of facial responses to noxious stimulation was verified. Furthermore, we found a significant main effect for ‘‘stimulus intensity’’ (see Table 2) with facial responses increasing across stimulus intensities (see Table 2 and Fig. 1). Moreover, the frequency and intensity of painrelevant AUs was significantly higher compared to the frequency and intensity of pain-irrelevant AUs as indicated by a significant main effect for ‘‘type of facial response’’ (see Table 2 and Fig. 1). Interestingly, the augmentation of pain-relevant responses compared to pain-irrelevant responses was
4
Self-report were ratings were classified as invalid when subjects did not respond at all or when their response did not fit to any of the categories of the verbal rating scale.
more pronounced in demented patients as indicated by a significant interaction effect between ‘‘group’’ and ‘‘type of facial response’’ (see Table 2 and Fig. 1). This finding clearly rejects the assumption of an unspecific overall increase of facial responses to noxious stimulation in demented patients (see hypothesis II); but rather suggests a pain typical increase of facial responses in patients with dementia. We also found a significant interaction between ‘‘group’’ and ‘‘stimulus intensity’’ (see Table 2). As can be seen in Fig. 1, the increase of facial responses across stimulus intensities was steeper in patients with dementia compared to healthy controls. Accordingly, facial responses encode stimulus intensities at least as well in demented patients as in healthy control subjects, which is contrary to hypothesis III. We also found a significant interaction between ‘‘stimulus intensity’’ and ‘‘type of facial response’’ (see Table 2). As can be seen in Fig. 1, pain-relevant facial responses increased steadily across stimulus intensities, whereas slopes of pain-irrelevant facial responses were more ambiguous. The interaction between all three factors was also significant (see Table 2), indicating that the dissimilarity of pain-relevant and pain-irrelevant stimulus-response slopes differed between demented patients and healthy controls. 3.2. Influence of dementia on self-report ratings Dementia had a strong effect on the capacity of the subjects to provide self-report ratings. Whereas healthy controls were able to continuously provide self-report ratings (100%), the percentage of stimuli that demented patients responded to with valid self-report ratings varied between 0% and 100% (mean value 91%). Furthermore, we found a highly significant correlation between the degree of cognitive impairment and the percentage of valid self-report ratings. With a decrease in
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Table 2 Results of the multiple analysis of variance for the effects of ‘‘group’’, ‘‘stimulus intensity’’ and ‘‘type of facial response’’ on composites scores for AUs frequency and intensity
Significant results are marked as bold.
4. Discussion The purpose of the study was to study facial responses to controlled noxious stimulation in demented patients and to determine if the typicalness of these responses for pain is changed in demented patients compared to cognitively unimpaired controls. We found, as claimed in our hypothesis I, that facial responses to pressure stimulation were significantly enhanced in demented patients compared to healthy
8 Healthy Controls Demented patients
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PAIN-RELEVANT
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b Healthy Controls Demented patients
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2 3 4 5 kg PAIN-RELEVANT
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Intensity of pain-irrelevant AUs
Frequency of pain-relevant AUs
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Frequency of the pain-irrelevant AUs
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controls. Demented patients displayed higher frequencies as well as higher intensities of facial responses. This finding is in accordance with previous findings. As described in the introduction, Hadjistavropoulos et al. [13] and Porter et al. [27] also reported that facial responses to potentially noxious procedures are increased in cognitively impaired elderly. This seems to be a very robust finding, given that all studies differed immensely with regard to pain induction methods (e.g. venipuncture [12] vs. experimental pressure pain), types of subjects (e.g. only patients with AD [27] vs. patients with AD, VD, MD) and selection of pain-relevant muscle movements (e.g. Porter et al. [27] included all AUs being displayed when forming a composite score, whereas we differentiated between pain-relevant and pain-irrelevant Action Units (AUs) (see Section 2 of this paper)). For readers, who are not familiar with the analysis of facial responses, we would like to stress that our selection of pain-relevant AUs – which aimed at guaranteeing pain-relevance for the present experimental stimulation – resulted in three out of four AUs, which have been introduced as ‘‘typical’’ pain AUs by Prkachin [28]. With regard to the typicalness of these amplified facial responses in demented patients for pain, we found that the amplification was mainly due to an increase of
Intensity of pain-relevant AUs
cognitive functioning (MMSE score), the ability to provide self-report ratings declined in demented patients (r = 0.681, p < 0.001). However, dementia had no significant main effect on the magnitude of self-report ratings of pressure stimulation (F(1,92) = 0.008, p = 0.929). As can be seen in Fig. 2 demented patients rated the stimuli (being of mild to moderate pain intensities) as painful as healthy individuals did. Furthermore, dementia did not interact significantly with the factor ‘‘intensity’’ (F(4,368) = 1.923, p = 0.106). This indicates that the increase of pain intensity ratings, which was significant across stimulus intensities (F(4,368) = 258.512, p < 0.001), did not differ between both groups.
0
PAIN-IRRELEVANT
Fig. 1. Composite scores of pain-relevant and pain-irrelevant facial responses (frequency (a) and intensity (b)) in demented patients and in healthy controls (Mean values (±SD)) to pressure stimulation.
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Verbal category scale
Healthy Controls Demented Patients
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Fig. 2. Self-report ratings in demented patients and in healthy controls (Mean values (±SD)) of pressure stimulation.
pain-relevant AUs. These are AUs, which occurred more often during ‘‘pain’’ than during ‘‘no-pain’’ in our experimental test both in patients with dementia and in healthy individuals and are also known as pain indicative from the literature [28]. When comparing the frequency and intensity of these pain-relevant AUs to the frequency and intensity of pain-irrelevant AUs, we found that pain-relevant AUs were even more frequent and intense compared to pain-irrelevant responses in patients with dementia than in healthy controls, thus clearly contradicting our hypothesis II. Consequently, our data clearly points out that the typicalness of facial responses for pain elicited by potentially noxious stimulation is not diminished in demented patients. Moreover, these facial responses proved as apt in demented patients as in healthy controls to encode the intensity of stimulation, thus falsifying our hypothesis III. In fact, the stimulus-response relationship appeared even more distinct in the patients than in the control subjects. These findings are very promising because they imply that nociception and pain are reflected as validly in the facial responses of patients with dementia as they are in cognitively unimpaired individuals. Therefore, the assessment of the facial expression of pain has the potential to serve as a valid alternative to self-report ratings in demented patients. This is of great relevance for pain assessment in dementia. In the last couple of years several attempts have been made to develop behaviorally based pain assessment scales for patients with dementia (for comprehensive reviews see [14,17,32]). Interestingly, all of these scales list the facial expression as an important behavioral pain indicator. However, most scales lack a definite description of how facial responses during pain exactly look like but provide rather vague descriptions such as ‘‘frowning’’, ‘‘grimacing’’, ‘‘looking tense’’ [17]. Our finding of a preserved pattern of facial responses in demented patients could possibly improve most of the behavioral pain assessment scales by giving more precise criteria for the assessment of the item ‘‘facial expression of pain’’ in demented patients.
Considering now again our finding of an augmentation of facial responses to noxious stimulation in patients with dementia, it might suggest an intensified processing of noxious stimulation in demented patients. This perspective was also given by a recent study on cerebral responses to noxious stimulation [2]. Cole et al. used functional magnetic resonance imaging (fMRI) to study cerebral activation during noxious stimulation in patients with dementia and reported that pain-related cerebral activations were significantly greater in demented patients compared to age-matched healthy controls. Thus, one can find indices for intensified processing of noxious stimulation in patients with dementia not only when looking at facial responses but also when assessing cerebral activation. However, it remains unclear whether an increased processing of noxious stimulation might also be associated with an amplified subjective pain experience in demented patients. Besides construing the increased facial responses in demented patients as an indication of intensified processing of noxious stimulation, alternative interpretations are also possible. It may well be that facial responses to noxious stimulation are increased simply because the cognitive ability in demented patients to control the impulse to display pain via facial responses is impaired. Cognitively unimpaired individuals are able to adjust the behavioral expression of internal states to given situations according to so-called display rules [6]. 4.1. Self-report ratings Another finding of our study was that some of the demented patients (N = 8) were not able to provide self-report ratings of pain continuously, although our experimental pain tests were non-demanding as regards cognitive capacities. This disability was significantly correlated to the degree of cognitive impairment. Similar findings have already been reported before (e.g. [13,21,22,25,26]) and it is meanwhile well known that the ability to give self-report ratings of pain is impaired in patients with dementia. These findings stress the urgent need for alternative pain assessment methods in order to validly assess pain in demented patients. As mentioned above, several attempts already have been made to develop observational pain assessment tools for demented patients. Those patients with dementia, who gave self-report ratings, rated the stimuli (being of mild to moderate pain intensities) as painful as healthy control subjects did. This finding is in accordance with previous studies, which also found that pain stimuli of mild to moderate intensities were rated equally painful by demented patients and healthy controls [1,9,27,29]. Is this clear evidence for an unchanged subjective pain sensitivity in demented patients? Not necessarily, since the psycho-
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metric quality (validity, reliability) of self-report ratings of pain in patients with dementia seem to be questionable, even if ratings are given. Future research has to solve the conflict between an apparently lowered – e.g. Benedetti et al. [1] reported on an increased pain tolerance in patients with Alzheimer’s disease – or unchanged processing of pain as suggested by verbal methods on the one hand and indices of an intensified processing as suggested by analyses of facial responses on the other hand. However, for the sake of patients with dementia, one should not be too fast in assuming less or no pain in this fragile patient group. 4.2. Limitations As described in the section on methods, cognitively unimpaired elderly subjects were recruited amongst students of the Senior University at the University of Marburg, which might have resulted in a ‘‘super-healthy’’ control group. However, when aiming at strictly excluding cognitive impairment it is nearly inevitable to select a group of well educated ‘‘super-healthy’’ older individuals, given that education as well as health has been shown to be related to the vulnerability for dementia (e.g. [23]). Furthermore, our statements regarding the typicalness of facial responses in demented patients for pain are solely based on investigating facial responses to pressure stimulation of non-painful and painful intensities. In order to prove the pain specificity of facial responses in demented patients beyond this point, it would be advisable to compare facial responses to noxious stimulation also with facial responses to other aversive stimuli. 5. Conclusion In conclusion, we found that facial responses to noxious stimulation were markedly increased in patients with dementia. Furthermore, we found that facial responses of demented patients to noxious stimulation encode the intensity of stimulation as well as facial responses of healthy individuals do. Moreover, our data clearly point out that the typicalness of these facial for pain responses is not reduced in demented patients. Therefore, the facial expression of pain has the potential to serve as an alternative pain indicator in patients with dementia, even in patients with more severe cognitive impairments and compromised selfreport. Acknowledgment This study was supported by a research grant of the Deutsche Forschungsgemeinschaft (La 685/5).
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[29] Rainero I, Vighetti S, Bergamasco B, Pinessi L, Benedetti F. Autonomic responses and pain perception in Alzheimers’s disease. Eur J Pain 2000;4:267–74. [30] Roman GC, Tatemichi TK, Erkinjuntti T, Cummings JL, Masdeu JC, Garcia JH et al. Vascular dementia: diagnostic criteria for research studies. Report of the NINDS-AIREN International Workshop. Neurol 1993; 43:250–260. [31] Smith M. Pain assessment in nonverbal older adults with advanced dementia. Perspect Psychiatr Care 2005;41: 99–113. [32] Zwakhalen SM, Hamers JP, Abu-Saad HH, Berger MP. Pain in elderly people with severe dementia: a systematic review of behavioural pain assessment tools. BMC Geriatr 2006;6:3.
The facial expression of pain in patients with dementia Miriam Kunz a,b,*, Siegfried Scharmann b, Uli Hemmeter b, Karsten Schepelmann c, Stefan Lautenbacher a b
a Physiological Psychology, Otto-Friedrich University Bamberg, Germany Department of Psychiatry and Psychotherapy, Philipps University Marburg, Germany c Department of Neurology, Philipps University Marburg, Germany
Received 26 April 2007; received in revised form 21 August 2007; accepted 10 September 2007
Abstract The facial expression of pain has emerged as an important pain indicator in demented patients, who have difficulties in providing self-report ratings. In a few clinical studies an increase of facial responses to pain was observed in demented patients compared to healthy controls. However, it had to be shown that this increase can be verified when using experimental methods, which also allows for testing whether the facial responses in demented patients are still typical for pain. We investigated facial responses in 42 demented patients and 54 aged-matched healthy controls to mechanically induced pain of various intensities. The face of the subject was videotaped during pressure stimulation and was later analysed using the Facial Action Coding System. Besides facial responses we also assessed self-report ratings. Comparable to previous findings, we found that facial responses to noxious stimulation were significantly increased in demented patients compared to healthy controls. This increase was mainly due to an increase of pain-indicative facial responses in demented patients. Moreover, facial responses were closely related to the intensity of stimulation, especially in demented patients. Regarding self-report ratings, we found no significant group differences; however, the capacity to provide these self-report ratings was diminished in demented patients. The preserved pain typicalness of facial responses to noxious stimulation suggests that pain is reflected as validly in the facial responses of demented patients as it is in healthy individuals. Therefore, the facial expression of pain has the potential to serve as an alternative pain assessment tool in demented patients, even in patients who are verbally compromised. Ó 2007 International Association for the Study of Pain. Published by Elsevier B.V. All rights reserved. Keywords: Dementia; Pain; Facial expression of pain; Non-verbal communication
1. Introduction It is well known that the capacity to report pain is diminished in demented patients and that especially patients with moderate to severe dementia have difficulties to provide self-report ratings of pain (for comprehensive reviews, see [16,17,31]). Based on these findings, many authors have stressed the urgent need for alternative non-verbal pain-assessment tools in order * Corresponding author. Address. Physiological Psychology, University of Bamberg, Markuspl. 3, 96045 Bamberg, Germany. Tel.: +49 951 8631850; fax: +49 951 8631976. E-mail address: [email protected] (M. Kunz).
to rule out the possibility of an under-detection of pain in this patient group (for comprehensive reviews, see [17,18,32]). Amongst others, the facial expression of pain has been suggested as a possible non-verbal alternative to self-report ratings [14,20]. The facial expression of pain is considered to be one of the most prominent non-verbal pain behaviors because of its reflexive nature, its salience and because it can be distinctively differentiated from other affective states [4]. So far, there are only four studies which focused on facial responses to potentially noxious procedures in elderly individuals with dementia [11–13,27]. Facial responses during flu injections [11], venipuncture [12,27] and exacerbation of chronic musculoskeletal
0304-3959/$32.00 Ó 2007 International Association for the Study of Pain. Published by Elsevier B.V. All rights reserved. doi:10.1016/j.pain.2007.09.007
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pain during physical exercise [13] were videotaped and later analyzed using the Facial Action Coding System [5]. Although the studies differed immensely with regard to the way in which pain was induced or varied, the findings are surprisingly homogeneous. First of all, it was consistently found that facial responses to potential noxious procedures intensify (compared to a baseline period) and can be assessed even in demented patients, who are verbally compromised [11–13,27]. Furthermore, it was reported that facial responses in demented patients are augmented compared to responses in cognitively unimpaired controls [13,27]. However, the authors also presumed that this augmentation of facial responses in demented patients was mainly due to a rather unspecific overall increase of facial responses [11,12,27]. This impression, though, was not based on a systematic analysis aiming at differentiating between pain-relevant and pain-irrelevant facial responses. Therefore, the question remains on how pain typical are facial responses to noxious stimulation in demented patients. Is dementia really associated with an augmentation of facial responses during pain which is part of a general disinhibition of facial responses? Moreover, no study before applied experimental pain stimuli – in order to exert exact control over the noxious input – when analyzing facial responses in demented patients. Our aim was to investigate facial responses of patients with dementia by testing three hypotheses experimentally: (I) Demented patients show more frequent and intense facial responses during potentially noxious stimulation than healthy individuals. (II) This relative increase is due to an unspecific overall increase of facial responses in demented patients. (III) Facial responses of demented patients encode the intensity of potentially noxious stimulation less well than facial responses of healthy individuals do.
2. Materials and methods 2.1. Subjects Forty-two patients with dementia (mean age 76.7 ± 7.3 years; $:22, #:20) and 54 healthy control subjects (mean age 74.2 ± 5.6 years; $:43, #:11) over the age of 65 participated in this study. Control subjects were recruited amongst students of the Senior University at the University of Marburg. Patients with dementia were recruited amongst inpatients from the Department of Neurology and the Department of Psychiatry and Psychotherapy of the University of Marburg. None had taken any analgesic medication for at least 24 h prior to the test session. Participants with any condition – other than dementia in the case of the patients – that could affect pain perception and pain report such as diabetes, hypertension, periph-
eral and central neuropathy, neurological and psychiatric disorders were excluded from the study. Prior to the experiment, a thorough neurological examination (including examination of the sensory system, testing of deep tendon reflexes, autonomic testing, sural neurography, etc.) was conducted in order to identify persons who met the exclusion criteria. Moreover, a neuropsychological examination was conducted to evaluate the cognitive status of the subjects. Amongst others, the Mini Mental State Examination test (MMSE), according to Folstein et al. [8], was used to assess the cognitive status. Patients with dementia had a mean MMSE-score of 16.3 (±5.5SD) and healthy controls had a mean score of 29.5 (±0.8SD). Furthermore, patients with putative dementia were examined by a neurologist or psychiatrist and diagnosed according to the criteria specified by the ICD-10, NINCDS-ADRDA [24] and NINDS-AIREN [30]. According to these diagnostic guidelines, analyses of cerebrospinal fluid, blood chemistry analysis, EEG, CT or MRT and ECG analyses were conducted besides clinical assessment. 16 patients met the NINCDSADRDA criteria for the clinical diagnosis of probable Alzheimer’s disease (AD), 17 patients met the NINDS-AIREN criteria for the clinical diagnosis of probable Vascular Dementia (VD) and 9 patients were diagnosed as suffering from Mixed Dementia (MD).1 The study protocol was approved by the ethics committee of the medical faculty of the University of Marburg. We took care that only patients with dementia were included in the study who still had legal capacity. After being informed in a slow and simple fashion, which was adjusted to the individual intellectual capacities, subjects gave written informed consent. We also provided instructions during testing as simple as possible and monitored the patients continuously for any signs of undue discomfort (verbally or non-verbally), in which case we stopped testing immediately. Healthy subjects were paid for participation. 2.2. Materials and procedure All testing were conducted during the hours of 3.00–6.30 p.m. and lasted for approximately 2 h. The testing procedure included an examination of potential exclusion criteria and neuropsychological examination (approximately 1 h), the experimental pain test (20 min), a short break (10 min) and an assessment of autonomic and motor reflexes (30 min, the results of which are not reported here). All subjects were seated in an armchair after the physical examination. Experimental pain was induced by using pressure stimuli. A Fischer algometer (a force gauge fitted by a rubber disk with a surface of 1 cm2) was used to apply noxious mechanical pressure [7]. The algometer was slightly modified so that each stimulus onset could be electronically recorded and could be used as a trigger signal for the video analysis. In order to familiarize subjects with pressure stimulation, three stimuli of 2 to 3 kg (‘‘kg’’ is used as physical unit in the present study because the Fischer algometer is scaled like that) were applied to the thigh before tests started. In the test 20 stimuli varying between 1 and 5 kg (4 stimuli at each inten-
1
Other forms of dementia were deliberately excluded.
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sity) were applied to the right and left forearm in a random order, which had been determined once and was used for all subjects. Pressure was increased steadily at an application rate of 1 kg per second until maximum stimulus intensity was reached and then continued at that level for another 5 s. Since maximum stimulus intensities varied between 1 and 5 kg, it took between 1 and 5 s to reach maximum intensity. The interval between stimulus applications varied between 20 and 30 s. Pressure application was always performed by the same experimenter, who had been trained in using the Fischer algometer. 2.3. Self-report Right after each stimulus application, subjects were asked to give self-report ratings regarding the peak sensation felt. Self-report was assessed via a 6-point verbal category scale (no pain – mild pain – moderate pain – strong pain – very strong pain – extremely strong pain). 2.4. Facial expression of pain The face of the subject was videotaped throughout the entire session. The camera was placed in front of the subject at a distance of approximately 4 m. Before applying a stimulus, subjects were always instructed to focus on an emotionally neutral picture being positioned behind the camera in order to ensure a frontal view of the face. Subjects were also instructed not to talk during pain induction. To mark the onset of pain stimulation on the videotape (for further analysis), we switched on a signal light concurrently. The light was visible to the camera but not to the subject. The Facial Action Coding System (FACS) [5] was used to analyze facial responses. The FACS is based on anatomical analysis of facial muscle movements and distinguishes 44 different action units (AUs). These are the minimal numbered units of facial activity that are anatomically separate and visually distinguishable. The intensity for each action unit was rated on a 5-point scale (A–E) with A being the least intense of the action and E the maximum strength of the action. A FACS coder (qualified by passing an examination given by the developers of the system) identified the frequency of all 44 AUs and the intensity of 42 AUs (AUs 45 and 46 do not allow for intensity coding). A special software designed for analysis of observational data (the Observer Video-Pro (Noldus Information Technology)) was used to segment the videos and to enter the FACS codes into a time-related data-base. Time segments of 5 s beginning just after stimulus and had reached maximum were selected for scoring. In total, 20 segments of pressure stimulation (4 series of pressure stimuli from 1 to 5 kg) were analyzed. For purpose of necessary data reduction, we combined those AUs that represent facial movements of the same muscle as has been done in preceding studies without any loss of information (e.g. [15,19,28]). Therefore, AUs 1 and 2, AUs 6 and 7, AUs 9 and 10 as well as AUs 25, 26 and 27 were combined to form new variables. To select those AUs that were pain-relevant in the present experimental context and to summarize these facial responses by computing a pain-relevant composite score, several steps were necessary.
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(1) As has been done in earlier studies (e.g. [3,10,13,19]), we denominated only those AUs as pain-relevant that occurred in at least 5% of the pain segments2 recorded. We did this separately for demented patients and healthy controls (the results are listed in Table 1)3. (2) To determine which of these AUs listed in Table 1 were critically more frequent during pain segments than during non-painful segments, we computed effect sizes (Cohen’s d for two dependant groups) for these differences. Effect sizes were computed separately for the demented patients and healthy controls. The values of these effect sizes are also listed in Table 1. For further analysis only those Action Units which reached an effect size d P 0.5 (medium effect) in both groups (these AUs are shaded in grey in Table 1) were used to form a composite score of pain-relevant facial responses. (3a) Prior to computing the composite score, the frequency values of all Action Units had to be given weights. This was necessary because the frequency of AU 45 (blinking of the eye) is disproportionally higher than those of the other AUs. In order to reduce this numerical distortion, we decided to compute weighted frequency values for all AUs. This was done by dividing the frequency of each AU at each stimulus intensity by the mean frequency of the given AU across all stimulus intensities. (3b) Composite scores of pain-relevant facial responses were formed by calculating mean scores of those AUs that proved to be pain-relevant (shaded in grey in Table 1) separately for each stimulus intensity and separately for FACS frequency and FACS intensity. (3c) We also computed composite scores of pain-irrelevant AUs by calculating mean scores of all AUs that did not prove to be pain-relevant. This was done to allow for the comparison between pain-relevant AUs and pain-irrelevant AUs, and thus evaluate the ‘‘pain typicalness’’ of facial responses. 2.5. Statistical analysis 2.5.1. Group differences in facial responses to pain To evaluate the impact of dementia on facial responses to pain, we computed a multiple (for frequency and intensity values) analyses of variance with repeated measurements on two within-subject factors ‘‘stimulus intensity’’(1 to 5 kg) and ‘‘type of facial response’’(pain-relevant and pain-irrelevant AUs) as well as with one between-subject factor ‘‘group’’(demented patients and healthy controls). In case of significant group difference, t-tests were computed for single comparisons. 2.5.2. Group differences in self-report To evaluate the influence of dementia on self-report ratings, we computed analyses of variance with repeated measurements on one within-subject factor ‘‘stimulus intensity’’ (1 to 5 kg) and with one between-subject factor ‘‘group’’(demented patients and healthy controls). 2
All trials being rated as ‘‘mild pain’’ or more on the verbal scale were considered to be pain segments. Trials rated as ‘‘no pain’’ were considered to be non-painful segments. 3 The selection of AUs in this step was based on these subjects, who were able to report pain by ratings (see Results for details).
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Table 1 Facial action units (AUs) with a critical occurrence of more than 5% in denominated ‘‘pain’’-segments in healthy controls and in demented patients (see text for further explanations)
a b
Percent denotes the percentage of occurrence in the entire pain segments. Blinking of the eye can appear more than once in a time-segment of 5 s. Relative frequency of occurrence and effect sizes for frequency differences between ‘‘pain’’ and ‘‘non-pain’’ segments are given. Medium and strong effect sizes (e P 0.5) are marked in bold; AUs shaded in grey represent AUs that were consistently more frequent (e P 0.5) during pain segments in both groups.
Furthermore, we were also interested in evaluating the extent to which dementia interferes with the capacity to provide self-report ratings. Therefore, we computed for each subject the percentage of stimuli that the subject responded to with valid self-report ratings4 and correlated these values with the degree of cognitive impairment (MMSE-score). Findings were always considered to be statistically significant at a < 0.05.
3. Results 3.1. Influence of dementia on facial responses to pain Dementia had a significant main effect on the frequency and intensity of facial responses to pressure stimulation (see Table 2). As can be seen in Fig. 1, the frequency and intensity of facial responses were markedly increased in demented patients. Single comparisons (T-tests) revealed that group differences were most evident for pain-relevant AUs (significant results are displayed in Fig. 1). Accordingly, hypothesis I about the effect of dementia on the frequency and intensity of facial responses to noxious stimulation was verified. Furthermore, we found a significant main effect for ‘‘stimulus intensity’’ (see Table 2) with facial responses increasing across stimulus intensities (see Table 2 and Fig. 1). Moreover, the frequency and intensity of painrelevant AUs was significantly higher compared to the frequency and intensity of pain-irrelevant AUs as indicated by a significant main effect for ‘‘type of facial response’’ (see Table 2 and Fig. 1). Interestingly, the augmentation of pain-relevant responses compared to pain-irrelevant responses was
4
Self-report were ratings were classified as invalid when subjects did not respond at all or when their response did not fit to any of the categories of the verbal rating scale.
more pronounced in demented patients as indicated by a significant interaction effect between ‘‘group’’ and ‘‘type of facial response’’ (see Table 2 and Fig. 1). This finding clearly rejects the assumption of an unspecific overall increase of facial responses to noxious stimulation in demented patients (see hypothesis II); but rather suggests a pain typical increase of facial responses in patients with dementia. We also found a significant interaction between ‘‘group’’ and ‘‘stimulus intensity’’ (see Table 2). As can be seen in Fig. 1, the increase of facial responses across stimulus intensities was steeper in patients with dementia compared to healthy controls. Accordingly, facial responses encode stimulus intensities at least as well in demented patients as in healthy control subjects, which is contrary to hypothesis III. We also found a significant interaction between ‘‘stimulus intensity’’ and ‘‘type of facial response’’ (see Table 2). As can be seen in Fig. 1, pain-relevant facial responses increased steadily across stimulus intensities, whereas slopes of pain-irrelevant facial responses were more ambiguous. The interaction between all three factors was also significant (see Table 2), indicating that the dissimilarity of pain-relevant and pain-irrelevant stimulus-response slopes differed between demented patients and healthy controls. 3.2. Influence of dementia on self-report ratings Dementia had a strong effect on the capacity of the subjects to provide self-report ratings. Whereas healthy controls were able to continuously provide self-report ratings (100%), the percentage of stimuli that demented patients responded to with valid self-report ratings varied between 0% and 100% (mean value 91%). Furthermore, we found a highly significant correlation between the degree of cognitive impairment and the percentage of valid self-report ratings. With a decrease in
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Table 2 Results of the multiple analysis of variance for the effects of ‘‘group’’, ‘‘stimulus intensity’’ and ‘‘type of facial response’’ on composites scores for AUs frequency and intensity
Significant results are marked as bold.
4. Discussion The purpose of the study was to study facial responses to controlled noxious stimulation in demented patients and to determine if the typicalness of these responses for pain is changed in demented patients compared to cognitively unimpaired controls. We found, as claimed in our hypothesis I, that facial responses to pressure stimulation were significantly enhanced in demented patients compared to healthy
8 Healthy Controls Demented patients
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controls. Demented patients displayed higher frequencies as well as higher intensities of facial responses. This finding is in accordance with previous findings. As described in the introduction, Hadjistavropoulos et al. [13] and Porter et al. [27] also reported that facial responses to potentially noxious procedures are increased in cognitively impaired elderly. This seems to be a very robust finding, given that all studies differed immensely with regard to pain induction methods (e.g. venipuncture [12] vs. experimental pressure pain), types of subjects (e.g. only patients with AD [27] vs. patients with AD, VD, MD) and selection of pain-relevant muscle movements (e.g. Porter et al. [27] included all AUs being displayed when forming a composite score, whereas we differentiated between pain-relevant and pain-irrelevant Action Units (AUs) (see Section 2 of this paper)). For readers, who are not familiar with the analysis of facial responses, we would like to stress that our selection of pain-relevant AUs – which aimed at guaranteeing pain-relevance for the present experimental stimulation – resulted in three out of four AUs, which have been introduced as ‘‘typical’’ pain AUs by Prkachin [28]. With regard to the typicalness of these amplified facial responses in demented patients for pain, we found that the amplification was mainly due to an increase of
Intensity of pain-relevant AUs
cognitive functioning (MMSE score), the ability to provide self-report ratings declined in demented patients (r = 0.681, p < 0.001). However, dementia had no significant main effect on the magnitude of self-report ratings of pressure stimulation (F(1,92) = 0.008, p = 0.929). As can be seen in Fig. 2 demented patients rated the stimuli (being of mild to moderate pain intensities) as painful as healthy individuals did. Furthermore, dementia did not interact significantly with the factor ‘‘intensity’’ (F(4,368) = 1.923, p = 0.106). This indicates that the increase of pain intensity ratings, which was significant across stimulus intensities (F(4,368) = 258.512, p < 0.001), did not differ between both groups.
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Fig. 1. Composite scores of pain-relevant and pain-irrelevant facial responses (frequency (a) and intensity (b)) in demented patients and in healthy controls (Mean values (±SD)) to pressure stimulation.
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Fig. 2. Self-report ratings in demented patients and in healthy controls (Mean values (±SD)) of pressure stimulation.
pain-relevant AUs. These are AUs, which occurred more often during ‘‘pain’’ than during ‘‘no-pain’’ in our experimental test both in patients with dementia and in healthy individuals and are also known as pain indicative from the literature [28]. When comparing the frequency and intensity of these pain-relevant AUs to the frequency and intensity of pain-irrelevant AUs, we found that pain-relevant AUs were even more frequent and intense compared to pain-irrelevant responses in patients with dementia than in healthy controls, thus clearly contradicting our hypothesis II. Consequently, our data clearly points out that the typicalness of facial responses for pain elicited by potentially noxious stimulation is not diminished in demented patients. Moreover, these facial responses proved as apt in demented patients as in healthy controls to encode the intensity of stimulation, thus falsifying our hypothesis III. In fact, the stimulus-response relationship appeared even more distinct in the patients than in the control subjects. These findings are very promising because they imply that nociception and pain are reflected as validly in the facial responses of patients with dementia as they are in cognitively unimpaired individuals. Therefore, the assessment of the facial expression of pain has the potential to serve as a valid alternative to self-report ratings in demented patients. This is of great relevance for pain assessment in dementia. In the last couple of years several attempts have been made to develop behaviorally based pain assessment scales for patients with dementia (for comprehensive reviews see [14,17,32]). Interestingly, all of these scales list the facial expression as an important behavioral pain indicator. However, most scales lack a definite description of how facial responses during pain exactly look like but provide rather vague descriptions such as ‘‘frowning’’, ‘‘grimacing’’, ‘‘looking tense’’ [17]. Our finding of a preserved pattern of facial responses in demented patients could possibly improve most of the behavioral pain assessment scales by giving more precise criteria for the assessment of the item ‘‘facial expression of pain’’ in demented patients.
Considering now again our finding of an augmentation of facial responses to noxious stimulation in patients with dementia, it might suggest an intensified processing of noxious stimulation in demented patients. This perspective was also given by a recent study on cerebral responses to noxious stimulation [2]. Cole et al. used functional magnetic resonance imaging (fMRI) to study cerebral activation during noxious stimulation in patients with dementia and reported that pain-related cerebral activations were significantly greater in demented patients compared to age-matched healthy controls. Thus, one can find indices for intensified processing of noxious stimulation in patients with dementia not only when looking at facial responses but also when assessing cerebral activation. However, it remains unclear whether an increased processing of noxious stimulation might also be associated with an amplified subjective pain experience in demented patients. Besides construing the increased facial responses in demented patients as an indication of intensified processing of noxious stimulation, alternative interpretations are also possible. It may well be that facial responses to noxious stimulation are increased simply because the cognitive ability in demented patients to control the impulse to display pain via facial responses is impaired. Cognitively unimpaired individuals are able to adjust the behavioral expression of internal states to given situations according to so-called display rules [6]. 4.1. Self-report ratings Another finding of our study was that some of the demented patients (N = 8) were not able to provide self-report ratings of pain continuously, although our experimental pain tests were non-demanding as regards cognitive capacities. This disability was significantly correlated to the degree of cognitive impairment. Similar findings have already been reported before (e.g. [13,21,22,25,26]) and it is meanwhile well known that the ability to give self-report ratings of pain is impaired in patients with dementia. These findings stress the urgent need for alternative pain assessment methods in order to validly assess pain in demented patients. As mentioned above, several attempts already have been made to develop observational pain assessment tools for demented patients. Those patients with dementia, who gave self-report ratings, rated the stimuli (being of mild to moderate pain intensities) as painful as healthy control subjects did. This finding is in accordance with previous studies, which also found that pain stimuli of mild to moderate intensities were rated equally painful by demented patients and healthy controls [1,9,27,29]. Is this clear evidence for an unchanged subjective pain sensitivity in demented patients? Not necessarily, since the psycho-
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metric quality (validity, reliability) of self-report ratings of pain in patients with dementia seem to be questionable, even if ratings are given. Future research has to solve the conflict between an apparently lowered – e.g. Benedetti et al. [1] reported on an increased pain tolerance in patients with Alzheimer’s disease – or unchanged processing of pain as suggested by verbal methods on the one hand and indices of an intensified processing as suggested by analyses of facial responses on the other hand. However, for the sake of patients with dementia, one should not be too fast in assuming less or no pain in this fragile patient group. 4.2. Limitations As described in the section on methods, cognitively unimpaired elderly subjects were recruited amongst students of the Senior University at the University of Marburg, which might have resulted in a ‘‘super-healthy’’ control group. However, when aiming at strictly excluding cognitive impairment it is nearly inevitable to select a group of well educated ‘‘super-healthy’’ older individuals, given that education as well as health has been shown to be related to the vulnerability for dementia (e.g. [23]). Furthermore, our statements regarding the typicalness of facial responses in demented patients for pain are solely based on investigating facial responses to pressure stimulation of non-painful and painful intensities. In order to prove the pain specificity of facial responses in demented patients beyond this point, it would be advisable to compare facial responses to noxious stimulation also with facial responses to other aversive stimuli. 5. Conclusion In conclusion, we found that facial responses to noxious stimulation were markedly increased in patients with dementia. Furthermore, we found that facial responses of demented patients to noxious stimulation encode the intensity of stimulation as well as facial responses of healthy individuals do. Moreover, our data clearly point out that the typicalness of these facial for pain responses is not reduced in demented patients. Therefore, the facial expression of pain has the potential to serve as an alternative pain indicator in patients with dementia, even in patients with more severe cognitive impairments and compromised selfreport. Acknowledgment This study was supported by a research grant of the Deutsche Forschungsgemeinschaft (La 685/5).
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