Emotional reaction in nursing home residents with dementia-associated apathy: A pilot study

Geriatric Mental Health Care 3 (2015) 1–6

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Geriatric Mental Health Care journal homepage: www.elsevier.com/locate/gmhc

Emotional reaction in nursing home residents with dementia-associated apathy: A pilot study Yvonne Treusch a,n, Julie Page a, Cornelis van der Luijt c, Mina Beciri c, Rebeca Benitez c, Maria Stammler c, Valentine L. Marcar b a

Zurich University of Applied Sciences, Institute of Occupational Therapy, Technikumstrasse 71, CH-8401 Winterthur, Switzerland Zurich University of Applied Sciences, Institute of Physiotherapy, Technikumstrasse 71, CH-8401 Winterthur, Switzerland c Kursana Residenz am Spisertor, Moosbruggstrasse, St. Gallen, Switzerland b

art ic l e i nf o

a b s t r a c t

Article history: Received 12 January 2015 Received in revised form 10 April 2015 Accepted 14 April 2015 Available online 8 May 2015

Introduction: Conventionally apathy is defined as a symptom primarily characterized by loss of feelings and emotional display and is the most common behavioural symptom in dementia patients. Neuronal network of emotions has ceased to function in patients suffering from dementia associated apathy. Objective and methods: We measured changes in skin conductance and heart rate from n ¼12 demented nursing home residents with clinical significant apathy (sumscore440 in the Apathy Evaluation Scale, AES) to images taken from the International Affective Picture System (IAPS, Lang et al., 2008). Additionally we used autobiographical material to study the responsiveness of the neuronal network of emotions and the adequacy of somatic indicators to demonstrate emotional reactions in individuals diagnosed with dementia and apathy. Results: Analysis of the EDA data revealed a significant difference in the change of skin conductance between the different image categories. The autobiographical material generated the largest change in skin conductance. Analysis of the heart rate did not yield any significant difference between the image categories. Conclusions: Our findings demonstrate that the neuronal network underlying emotion is still responsive in patients diagnosed with dementia associated apathy, although residents don't seem to be involved emotionally from an extraneous visual focus. Non pharmacological therapy approaches should deal with individual, familiar, autobiographic material to ensure a high level of emotional response and therefore reduce apathy severity. & 2015 Elsevier GmbH. All rights reserved.

Keywords: Ageing Cognition Autonomous nervous system Degenerative illness

1. Introduction Apathy is a term used by the Stoic philosophers to refer to the worthwhile condition of being free from emotions and passions. Today the term “apathy” refers to a loss of motivation, interest and concern and with a prevalence rate between 30–82% in dementia subjects. Prevalence rates vary depending on dementia severity, setting and assessment used, nevertheless apathy is considered the most common behavioral symptom in dementia (Boyle et al. 2005; Majic et al., 2010; Savva et al., 2009). Apathy causes clinically relevant changes in occupational and social interactions (Starkstein and Leentjens, 2008). It places a greater burden on caregivers and might be a major stressor than many active neuropsychiatric behavioral symptoms (Kaufer et al., 1998). As it responds poorly to treatment, increased disability and reduced independence in activities of daily living are frequent

n

Corresponding author.

http://dx.doi.org/10.1016/j.gmhc.2015.04.001 2212-9693/& 2015 Elsevier GmbH. All rights reserved.

consequences (Brodaty and Burns, 2011). Added to this, is the distress experienced by caregivers on how best to interact with such patients (Kaufer et al., 1998). In spite of its prevalence and clinical significance, apathy is still poorly represented in the psychiatric disease classification systems. In addition there is an absence of evidence and guideline suggestions for dealing or treating apathy adequately. A lack of understanding and assessing apathy may lead caregivers and clinicians to “misinterpret the apathetic behavior, as laziness, deliberate opposition or lack of interest” (Landes et al., 2005, p 342). Apathy is a multifaceted syndrome with affective, cognitive and behavioural components (Njomboro and Deb, 2014). Disturbance of affective-emotional processing seems to be the first in the series of three stages associated with apathy followed by disturbances of cognitive and auto-activation processing (Clarke et al., 2008; Seidl et al., 2007; Starkstein et al., 2006). As a diagnostic criterion of apathy Robert et al. (2009) suggest a loss of or diminished display of emotion. Similarly, Marin (1991) defines apathy as a lack of motivation, characterized by diminished

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goal-directed motor behavior, goal-directed cognition and emotional response. The loss of emotions that accompanies apathy is characterized by a blunting and flattening of affective responses (Sims, 2003). Other authors object, that the affective dimension of apathy is an interpretation more than an objective observation and therefore define the symptom as a “quantitative reduction of self-generated voluntary and purposeful behavior” (Levy and Dubois, 2006, p 916). Studies on clinical affective correlations of apathy paint a heterogeneous picture (Boyle et al., 2003): The inclusion of the emotional dimension as part of the definition of apathy has recently been called into question (Starkstein and Leentjens, 2008). To date, measurement of emotions has not been regularly correlated with measurements of apathy in dementia patients. In part this is due to the absence of valid operationalization of emotional functioning in this patient group. Another barrier is the difficulty in assessing emotional functioning in this patient group, as in most cases the assessment is confounded by the fact that many dementia patients receive medication, such as neuroleptics to treat agitation. Such medication modulates dopaminergic neurotransmission (Majic et al., 2010): Both generations of medication (first and second generation antipsychotics) tend to block D2 receptors in the dopamine pathways of the brain. This means that dopamine released in these pathways has less effect. Dopamine regulates several physiological processes in the central and peripheral nervous systems and is associated with executive behavior control and cognition. A dysfunction of these neurocircuits is associated with impairments in motivation that underlie symptoms of apathy (Heinz et al., 1998). Neuroleptic medication impairs dopaminergic stimulation even further (Majic et al., 2010). Beside this, antipsychotics are combined with a fairly large increase in serious other adverse events in dementia. Guidelines for the management of neuropsychiatric symptoms in dementia in general recommend non-pharmacological interventions as treatment option of first choice. In contrast, there is a lack of concrete suggestions for the treatment of a specific symptom, like apathy due to methodological limitations of the guideline-included studies (Vasse et al., 2012). Nursing home staff and therapists often feel helpless and frustrated when dealing with patients displaying apathy and do not know how to improve their motivation and general well-being: Apathetic patients often show hardly any internal motivation to act and rarely any reaction to external stimuli. So it can be unsatisfactory and discouraged for staff to interact with them. Knowing whether their emotional experience is still intact would give important information about their personal preferences for certain activities. Emotions are also the main indicators of affective disorders and an important source of information about their well-being (Vos et al., 2012). Because of communicative and cognitive limitations, relying on self-reports in this patient group to identify their emotional experience is problematic. Somatic indicators (e.g. changes in skin conductance, pupil size or heart rate) have proven an effective and reliable source of information about the function of the neuronal mechanism of emotions in healthy subjects, as they are triggered by the autonomic nervous system (Oliveira-Silva and Goncalves, 2011). Such indicators can serve as a means to assess emotional processing in nursing home residents suffering from dementia associated apathy. Heart rate and skin temperature have been reported to indicate the emotional state of individuals with severe and profound intellectual disabilities (Vos et al., 2012). To date there are no studies investigating whether these indicators are applicable and valid in dementia subjects. We were interested in whether affective reactions can be shown in humans with dementia associated apathy and whether these emotional responses differ between different stimuli. The

pilot study served as a proof-of-concept for a cohort study, aimed at addressing the following questions:

 Are somatic indicators (changes in skin conductance and heart 

rate) adequate to demonstrate emotional reactions in this patient group? Can emotional reactions in this patient group be elicited using standardized pictures from the IAPS (International Affective Picture System; Lang et al., 2008)?

In the work reported here, we examined affective reactions in dementia patients with apathy to pictures from the International Affective Picture System (IAPS; Lang et al., 2008) and contrasted their affective reactions to autobiographic material. An additional aim of the pilot study was to provide care-giving and management staff at the nursing home information on the participant's emotional reactions to different stimuli.

2. Materials and methods 2.1. Participants A power analysis performed using GPower (Ver. 3.1; A. Bucher, University of Kiel, Germany), yielded a study population size of 10. Assuming a drop-out of 25% we increased this to 12 participants. The 12 participants (10 females) were recruited from a residential and nursing home in Switzerland. Their average age was 89.75, range 77–97. All were diagnosed with mild to severe dementia and exhibited apathetic behavior, as assessed using the German version of the Apathy Evaluation Scale (AES) (Lueken et al., 2006). Participants had an AES score of 40 and above. We independently assessed cognitive ability using the Mannheim implementation of the Mini-Mental Test (Arbeitsgruppe Psychogeriatrie, ZI Mannheim, J 5, D-68159 Mannheim, Germany). The mean MMS was 12.2, range 0–25. The protocol was approved by the ethics committee of the canton St. Gallen (EKSG 13/066). In addition, consent was obtained from close family members or legal representatives. 2.2. Electrodermal activity and heart rate measurement Electrodermal activity (EDA) was measured by placing an electrode each on the middle (D3) and ring finger (D4) and connecting them to an amplifier (QuickAmp, MES, Gilching, Germany). Heart rate (HR) was measured using an infra-red blood-oxygen saturation sensor (SaO2) attached to the index finder (D2). EDA and HR were recorded at a frequency of 125 Hz using commercial software (Vision Recorder Ver 1.2; Brain Products, Munich, Germany) and stored on the hard disk drive of a laptop PC. 2.3. Stimulus material We selected images from the categories “Valence” (ranging from pleasant to unpleasant) and “Arousal” (ranging from calm to excited) of the International Affective Picture System (IAPS; Lang et al., 2008). In each case the chosen pictures had the largest SAMscore (Self-Assessment Manikin, SAM, an affective rating system devised by Bradley and Lang, 2002), a 9-point rating scale for each dimension in their respective category in a norm sample: Three pictures were chosen with a maximum norm score in Valence, three with a neutral score and three with a minimum score and the same for Arousal. The IPAS identification number of each image, as well as its Valence and Arousal score is listed in Table 1. In addition we included autobiographic material which was obtained from close family members. All material was presented a

Y. Treusch et al. / Geriatric Mental Health Care 3 (2015) 1–6

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Table 1 The table shows the IAPS image number and their Valence and Arousal sore of the images used. The standard deviations are shown in brackets. The two left most columns show the mean Valence and Arousal score of the images in each category. (A neural score is given the value 4.). Category

Image #

Valence (SD)

Arousal (SD)

Image #

Valence (SD)

Arousal (SD)

Image #

Valence (SD)

Arousal (SD)

Valence þ Valence 0 Valence  Arousal þ Arousal 0 Arousal 

1460 1390 3180 1050 6837 7004

8.21 4.50 1.95 3.46 4.25 5.04

4.31 5.29 5.95 6.87 4.50 2.00

1710 2383 2703 4650 5982 7020

8.34 4.72 1.91 6.96 7.61 4.97

5.41 3.41 5.78 5.67 4.51 2.17

2070 2393 9940 9410 7510 7175

8.17 4.87 1.62 1.51 6.05 4.87

4.51 2.93 7.15 7.07 4.52 1.72

(1.21) (1.56) (1.22) (2.15) (1.53) (0.60)

(2.63) (1.97) (2.95) (1.68) (2.06) (1.66)

(1.12) (1.36) (1.26) (1.54) (1.48) (1.04)

photographic image and processed using ImageJ (W. Rasband, NIH, USA) so that they had the same spatial dimensions and comparable mean luminance. 2.4. Paradigm Most measurements took place before noon but investigators followed the resident's subjective time preferences. Participants were measured in their room of residence and whenever possible seated in a chair with an unobstructed view to the PC screen. Four participants were measured in a reclining position in their bed. Participants were then informed about the nature of the measurements to be made and shown both the electrodes and the SaO2sensor. All measurements were conducted in the presence of a senior member of the nursing home staff. The EDA electrodes were first attached and connected to the recording PC, followed by the SaO2-sensor. Registration of the EDA and HR was then initiated. The paradigm was programmed in Presentation Ver. 13 (NBS, Berkeley, CA, USA) running under Windows XP with Service Pack 2 (Microsoft Corp, Redmond, WA, USA) on a laptop PC. Image category was randomised using a Latin square procedure. Each image was presented for 15 s and followed for 10 s by a uniform grey image. The onset of each image was identified in the EEG-data by a unique marker. Once started the sequence of images continued uninterrupted until all images had been displayed. During the measurement, the participant's gaze was continuously observed by the member of the nursing staff throughout and if their attention drifted, they reminded them to observe the screen. When the presentation of the image series concluded, EDA and HR ceased and the electrodes and SaO2– sensor removed. The participant was then asked if they had recognised anyone or anything in the images they had seen. This concluded the measurement session. 2.5. Data analysis Pre-processing of both EDA was performed using Analyzer Ver. 2 (Brain Products, Munich, Germany). Pre-processing of the EDA data commenced with bandpass filtering of the data using a lower cut off of.016 Hz and an upper cut off of 5 Hz. This was followed by applying a baseline correction with the 1 s period preceding each marker serving as the reference. We then extracted data segments 8 s in length and averaged the segments for each image category to obtain the mean EDA response to that category. The mean EDA for each category was saved in ASCII format. Subsequent analysis was performed using Microsoft Excel 2013 (Microsoft Corp. Redmond, WA, USA). For each participant we normalised the mean EDA response, by dividing each data point by the maximum obtained across all conditions from that participant. The small sample size in our study, may not have resulted in normally distributed data set. We therefore opted to analyse our EDA responses using the non-parametric, Friedman analysis of variance by rank test, as implemented by SPSS 20 (IBM, New York, NY, USA).

(2.34) (1.83) (2.25) (2.14) (2.85) (1.71)

(1.46) (1.06) (1.20) (1.15) (1.6) (1.00)

(2.74) (1.88) (2.24) (2.06) (2.35) (1.26)

8.24 4.70 1.83 3.98 5.97 4.97

4.73 3.88 6.30 6.54 4.51 1.96

Starting at each marker we divided the heart rate data into 8 s long segments. These segments were saved in ASCII format and then analysed further using Microsoft Excel. For each participant and image category, we calculated the coefficient of variation (CoV) of the inter-beat interval (IBI), based on the peak to peak interval. The CoV to the different image categories were compared using a Friedman analysis of variance by rank test as implemented by SPSS 20.

3. Results All participants displayed some sort of emotional response to the autobiographical material. This response varied from a change in facial expression to a clapping of their hands and exclamations of joy. This reaction was accompanied by changes in skin conductance but not heart rate. No such responses were forthcoming when viewing the IAPS material. Any such emotional reaction was either absent or so subtle that it was not perceived. However, IAPS images did induce changes in skin conductance but not heart rate. Fig. 1 depicts the relative change in skin conductance to each image category. Analysis of the EDA data revealed a significant differences in the change of skin conductance between the different image categories (df ¼6, p¼ .019). Fig. 2 shows the normalised peak amplitude to each image category. The error bars represent one standard error of the mean. The graphs show that the autobiographical material generated the largest change in skin conductance. The mean amplitude of the change in EDA increased with the mean “Valence” score to the IAPS images in our “Valence” category. The mean amplitude of the EDA change however varied inversely with the mean “Arousal” score of the images in our “Arousal” category (See Fig. 2). The amplitude of the EDA change did not reflect the mean “Arousal” score of the images in the “Valence” category nor did it reflect the mean “Valence” score of the images in the “Arousal” category. Analysis of the heart rate did not yield any significant difference between the image categories using either inter-beat interval (IBI), CoV of the IBI or peak amplitude (Fig. 3).

4. Discussion Apathy in patients with dementia has been linked to reduced efficacy of affective-emotional processing (Clarke et al., 2008; Seidl et al., 2007; Starkstein et al., 2006). The aim of our investigation was therefore, to study the responsiveness of the neuronal network of emotions and to determine the usefulness of somatic indicators to reveal emotional reactions in individuals diagnosed with dementia and apathy. The presence of emotional reactions when viewing autobiographic material and the associated changes in skin conductance in this patient group answers both questions in the affirmative. The absence of obvious emotional reaction coupled with the presence of somatic reactions to IAPS images merits closer examination.

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Normalisedgrand mean amplitude(% max) 50 40

Amplitude

30 20 10 0 -10

4

504 1004 1504 2004 2504 3004 3504 4004 4504 5004 5504 6004 6504 7004 7504

-20 -30

Time (ms) Autobiographic Valence -ve

Arousal -ve Valence 0

Arousal 0 Valence +ve

Arousal +ve

Fig. 1. Normalised change in skin conductance.

Normalised peak grand meanamplitude 70 60 50 40 30 20 10 0

Autobiog. Arousal -ve

Arousal 0 Arousal +ve Valence -ve Valence 0 Valence +ve

Image category Fig. 2. Normalised peak grand amplitude in skin coductance.

Inter-beat interval (IBI) 250

IBI (ms)

230 210 190 170 150 Autobiog.

Arousal -ve

Arousal 0

Arousal +ve

Valence -ve

Valence 0

Valence +ve

Image Category Fig. 3. Heart rate  inter-beat interval (BI).

Skin conductance change is a manifestation of the response of the autonomous nervous system. The autobiographic image material can be assumed to have had both a high arousal and a high positive valence for an individual. The former is borne out by the observed reactions when such material was presented. The presence of a more pronounced EDA change to IAPS images with a positive “Valence” score concurs with the findings of Rösler et al. (2005). They reported a “weakened sustained attention towards negative but not positive emotional pictures in the elderly”, in line with the socio-emotional selectivity theory suggesting a relative selection of positive stimuli with of advanced

age. However the EDA change observed to the IAPS images with a positive “Arousal” score were clearly smaller than that to IAPS images with a negative “Arousal” score. Comparing the EDA change with the “Arousal” score of the images of the “Valence” group did not yield any correspondence, nor did its comparison with the “Valence” score of the images in the “Arousal” group. Taken together with the findings of Rösler and colleagues our observations point towards the presence of distinct neuronal mechanisms of attention; a non-hedonic mechanism driven by the arousal a stimulus generates and a hedonic mechanism driven by the valence of a stimulus.

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While some authors have concluded that emotional reactions to stimuli are better reflected in changes in heart rate of healthy young volunteers rather than in changes of skin conductance (Oliveira-Silva and Goncalves, 2011), we found the opposite to be the case. Whether this is related to differences in methodology, age or cognitive ability of the study population needs to be examined in future research. Autonomic activity as a biomarker for cognitive impairment has been reported to vary with age (Giblin et al., 2013). Further, patients with severe dementia exhibit a decreased variability in their heart rate (Giblin et al., 2013; Phillips, 2011). Whether and how these factors influenced our findings needs to be addressed in future research. Although nursing home residents with severe dementia related apathy often appear to lack any reaction to external stimuli, our findings indicate that the neuronal network serving emotions responds differentially to external stimuli. Knowing that the neuronal network of emotion of patients displaying apathy reacts to stimuli evoking emotions is an essential insight for both family members and care professionals when dealing with this condition. For family members it indicates that their presence, serves as an autobiographic stimulus, and so has the utmost relevance to the patient. For caregivers in nursing and residential homes, it implies that their action and interaction do evoke an emotional response, even if it is not externalised. Our findings also imply that the emotional and social needs of a person with dementia persist even when apathy dominates. They should be addressed within psychosocial interventions, as stated by guidelines dealing with the treatment of dementia and neuropsychiatric symptoms (AGS & AAGP, 2003; DGPPN and DGN, 2009). Socio-therapeutic interventions such as occupational therapy therefore play an important role in improving the quality of life of this patient group (Treusch et al., 2011). Such interventions should include “activities therapy, modification of activities of daily living care to meet individuals' needs, environmental modifications, behavioral theory treatments, and social contact interventions.” (AGS & AAGP, 2003). In order to do justice to the emotional needs it is important to gain as much information about the personality, life history and interests as possible. Emotional responses to autobiographic material (for example photos of relatives or pets) are an important therapeutic resource. Care givers should use these emotional resources for therapeutic intervention to improve motivation and drive. Besides, studies dealing with emotional experience in mild to moderate AD suggest that a huge number of different materials (for example familiar films, pictures, stories, music) can be used for the induction of positive feelings (Blessing et al., 2014). Our findings underline the importance of this passive symptom and assess and treat it adequately (for assessing and treatment see consensus statement of the AGS & AAGP, 2003), because current research states, that more active behavioral symptoms are more often realized and treated by nursing home staff (Colling, 1999; Leone et al., 2013). Determining emotions in people with severe dementia is as important as challenging: since self-reports are not always reliable, observable behavior is the most used source of information. Given the limited externalized display of emotions in apathy affected patients, it is prudent to supplement observations with information from additional sources.

5. Conclusion In patients diagnosed with dementia and exhibiting apathy, the neuronal network underlying emotion is responsive. At present, there is no consensus whether heart rate variability, skin conductance or temperature is a more reliable somatic indicator. Clarifying this issue deserves high priority in future research.

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Our study has shown that autobiographic material is more effective than standardised emotive pictures. The use of autobiographic material with positive associations for occupational therapy and care are highly relevant in nursing home residents suffering from dementia associated apathy.

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