Reduced Empathy Scores in Patients with Parkinson’s Disease: A Non-Motor Symptom Associated with Advanced Disease Stages

Abstract

Background:

Empathy describes the ability to infer and share emotional experiences of other people and is a central component of normal social functioning. Impaired empathy might be a non-motor symptom in Parkinson’s disease (PD).

Objective:

To examine empathic abilities and their relationship to clinical and cognitive functioning in PD patients.

Methods:

Empathy was measured in 75 non-demented PD patients and 34 age-matched healthy controls using a German version of the Interpersonal Reactivity Index. Moreover, we collected demographic and clinical data and conducted a comprehensive neuropsychological test battery.

Results:

PD patients had a significant lower global empathy score than healthy controls. Furthermore, we found significant group differences for the cognitive empathy scales but not for the scales which are sensitive for affective empathy components. The empathy decrease was significantly higher in advanced Hoehn & Yahr stages. There were only sporadic significant correlations between empathy scores and cognitive variables.

Conclusions:

PD patients show a stage dependent empathy score decrease which is driven mainly by cognitive aspects of empathy. However, emotional empathy aspects are not reduced.

Keywords

Parkinson’s disease empathy Theory of Mind Interpersonal Reactivity Index

INTRODUCTION

The characteristic motor symptoms in Parkinson’s disease (PD) are often accompanied by autonomic, sensory, cognitive, or behavioural symptoms. These non-motor symptoms are particular relevant because they show a high prevalence [1] and a significant association with quality of life [2].

In this study, we focus on empathy as an issue of affective experience and a central component of social functioning. The term ‘empathy’ describes the ability to infer and share the emotional experiences of other people [3]. A general problem in the empathy research seems to be the lack of clear definitions and vague conceptual differentiations. Several terms like “Theory of Mind” [4], “Mentalizing” [5, 6], “Mind-Reading” [7], for example, were partially used as synonyms for empathy. We adopt a concept formulated by Singer [8] that proposed to disentangle the concept of empathy from those of the others. The authors defined Theory of Mind (or Mentalizing/Mind-reading) as the cognitive ability to represent other people’s desires, beliefs, or intentions. Empathy, however, includes an additional understanding and experiencing of other people’s emotions by sharing their affective state. Therefore, empathy comprises both a cognitive perspective taking and an own emotional reaction due to getting into another’s mind and ToM can be effectively seen as a precondition for empathy. Empathic reactions can be self-oriented (e.g., discomfort, pleasure, sadness, anxiety) or directed at other people (e.g., warmth, sympathy, compassion, concern) and are accompanied by bodily sensations which is an important feature to distinguish empathy from ToM. Evidence for a conceptual differentiation between ToM and empathy arise from studies which showed that they are based on different neuronal structures. While ToM tasks seems to be associated with the anterior paracingulate cortex, the superior temporal sulcus and the temporal poles [9], empathy seem to rely on sensorimotor cortices and (para-)limbic structures [8].

Even though affective non-motor impairments like apathy, anxiety, or depression are well described and also deficits in the related ToM concept have frequently been demonstrated in patients with PD [10, 11], the emotional aspect of empathizing has been widely ignored in PD research so far. Here, we hypothesized disease related alterations of empathy in PD using an established empathy questionnaire on a large sample of patients and healthy controls.

METHODS

Seventy-five patients with idiopathic PD diagnosed according to the United Kingdom Parkinson’s Disease Society Brain Bank criteria [12] as well as 34 healthy controls were included in this study. Exclusion criteria were any neurological disease other than PD, deep brain stimulation, and dementia according to the Parkinson’s disease dementia criteria [13]. The study was approved by the local ethics committee. All participants gave written informed consent to participate in the study. Demographic and clinical characteristics of the study sample are given in Table 1.

Table 1

Sociodemographic and clinical characteristics and IRI empathy scores of PD patients and healthy controls

	PD (n = 75)	HC (n = 34)	Z	p value
Age	64.1±8.2	63.3±6.7	–0.929	0.363
Sex (M/F)	45/30	14/20	2.148 (χ²)	0.096
MMSE	28.6±1.9	28.8±1.2	–0.881	0.324
Geriatric Depression Scale	3.27±3.0	1.15±1.08	–3.733	0.000
Disease duration (years)	6.1±5.1
UPDRS III	19.8±10.9
L-dopa equivalent daily dose (mg)	691.1±375.9
Hoehn &Yahr	I: 18; II: 32; III: 22; IV: 3
Global Empathy Score	39.7±7.5	44.1±7.2	–2.779	0.007
Empathic concern	14.4±2.7	15.0±2.7	–1.333	0.184
Personal distress	10.5±3.5	10.1±3.4	–0.425	0.568
Fantasy	11.2±3.6	13.3±3.2	–2.830	0.007
Perspective taking	14.1±2.8	15.8±2.8	–3.029	0.004

Data are given as mean±standard deviation; IRI: Interpersonal Reactivity Index; PD: Parkinson’s disease, HC: Healthy controls; MMSE: Mini Mental Status Examination; UPDRS: Unified Parkinson’s Disease Rating Scale. Group comparisons were calculated using Mann Whitney U tests or Fisher’s exact test. Significant results are in bold.

To assess the ability to empathize, we used a validated German version of the Interpersonal Reactivity Index (IRI) from Davis [14] (Saarbrücker Persönlichkeitsfragebogen [15], v.5.4). This questionnaire contains 16 statements and the test person has to decide to what extent these statements apply on a five-point scale ranging from 0 (applies not at all) to 4 (applies very well). The questionnaire includes four subscales, each covering a different aspect of empathy. The Empathic Concern scale measures reactive feelings of sympathy and concern for unfortunate others (e.g., “I often have tender, concerned feelings for people less fortunate than me”). The Personal Distress scale assesses feelings of anxiety and unease in tense interpersonal settings (e.g., “I sometimes feel helpless when I am in the middle of a very emotional situation”). The Fantasy scale aims to measure the tendency to transpose oneself imaginatively into the feelings of fictitious characters in books and movies (e.g., “When I am reading an interesting story or novel, I imagine how I would feel if the events in the story were happening to me”). The last scale, Perspective Taking, assesses the tendency to adopt the psychological point of view of others (e.g., “I try to look at everybody’s side of a disagreement before I make a decision”). A global empathy score calculated by summing up all four subscores is not reasonable. D’Orazio [16] argues that the four subscales are not all positively correlated and therefore increases in every subscale are not considered indicative of greater empathy levels. Furthermore, the validity of the PD dimension was called into question by the results of a factor analytic study [17]. The authors proposed the summation of Empathic Concern, Perspective Taking, and Fantasy as a measure of general empathic disposition. The validity of this score was demonstrated in the German version of the IRI as well [18].

The Mini Mental State Examination (MMSE [19]) was used as a screening instrument for global cognitive functioning. Disease severity was rated with the Unified Parkinson’s disease rating scale (UPDRS) III [20] and graded according to the Hoehn & Yahr stages [21]. The 15-item version of the Geriatric Depression Scale (GDS [22]) was used to measure depression. In addition, an extensive neuropsychological test battery including tests to assess the following cognitive domains was conducted:

memory (Consortium to Establish a Registry for Alzheimer’s Disease/CERAD [23, 24]: Word list Learning and Recall),

attention (Brief Test of Attention [25]; Stroop Test [26]: reaction time),

executive functions (CERAD: lexical and phonemic fluency tests, Trail Making Test; Wechsler Memory Scale – Revised [27]: Digit Span backward; Modified Card Sorting Test [28]: categories completed and perseverative errors; Stroop Test: errors),

visual-spatial functions (CERAD: Constructional praxis; Leistungsprüfsystem 50 + [29]: Subtests 7 and 9), and

language (CERAD: Boston Naming Test).

All statistical analyses were carried out using SPSS 21 (IBM SPSS Statistics for Windows. Armonk, NY: IBM Corp.). Given the fact that most variables did not fulfil the requirements for parametric testing (only 3 out of 29 collected variables showed both a normal distribution in both groups and homogeneity of variance), we entirely used nonparametric statistical tests aware of the increased risk of type 2 errors in these variables. For group comparisons between two groups we conducted Mann-Whitney U tests respective Fisher’s exact tests. To analyse group differences between more than two groups, we used Kruskal-Wallis tests. A significant result triggered pairwise Mann-Whitney U tests corrected for multiple comparisons (Bonferroni correction). The level of significance was set at 0.05 for each test. To reveal associations between empathy scores and clinical as well as cognitive variables we used the nonparametric Spearman’s rank correlation coefficient. Due to the large number of tests in the correlation analysis, we set the significance to a more conservative level of 0.01.

RESULTS

Patients and healthy controls did not significantly differ in terms of age, gender distribution, and global cognitive functioning as measured by the MMSE. PD patients showed a significant lower global empathy score than healthy controls. The analysis of the four subscales showed significant group differences for the scales Fantasy and Perspective Taking (Table 1). Comparing healthy controls and PD patients grouped on the basis of their Hoehn & Yahr (H&Y) stage, we found significant differences between healthy controls and PD patients in H&Y stage III for the global empathy score as well as for the subscales Fantasy and Perspective Taking (Table 2). No significant differences were evident between controls and patients in earlier stages of the disease (H&Y I and II). Furthermore, PD patients in H&Y stage III scored significantly lower than PD patients in H&Y stage I on the same scales. Disease duration correlated significantly negatively with the global empathy score (r = –0.359, p = 0.002) and the subscales Fantasy (r = –0.309, p = 0.007) and Perspective taking (r = –0.319, p = 0.005). Empathic Concern and Personal Distress did not correlate with any clinical variable. Furthermore, we calculated a partial correlation between disease duration and empathy with l-dopa equivalent daily dose as control variable. The correlations were no longer significant (p > 0.1). The partial correlations between dopa equivalent daily dose and empathy controlled for disease duration failed to reach significance on the 0.01 level in the fantasy scale (r = –0.250, p = –0.25) as well as in all other empathy scores (p > 0.1). The GDS correlated significantly with the Personal Distress scale (in patients) respective with the Perspective Taking scale (in controls). We only found sporadic significant correlations between empathy scores and cognitive variables which cannot be meaningfully interpreted. The results of the correlation analysis can be seen in Supplementary Table 1.

Table 2

IRI empathy scores for healthy controls and PD patients separated for Hoehn & Yahr stage I to III

	HC (n = 34)	H&Y I (n = 19)	H&Y II (n = 32)	H&Y III (n = 21)	χ²*	p*
Global Empathy Score	44.1±7.2^a	42.6±4.8^b	40.6±8.0	35.3±6.7^a,b	18.44	0.000
Empathic Concern	15.0±2.7	15.1±1.3	14.3±3.0	13.6±2.8	5.90	0.117
Personal Distress	10.1±3.4	10.5±2.9	10.9±4.0	9.7±3.1	1.44	0.697
Fantasy	13.3±3.2^a	12.7±3.6^b	11.8±3.4^c	9.1±3.3^a,b,c	17.37	0.001
Perspective Taking	15.8±2.8^a	14.8±1.9^b	14.4±3.0	12.7±2.4^a,b	16.77	0.001

Data given as mean±standard deviation. IRI: Interpersonal Reactivity Index; HC: Healthy controls, H&Y: Hoehn & Yahr stage. *Kruskal-Wallis omnibus test was performed to identify significant group differences in the dataset of all 4 groups. Significant test results (in bold) triggered a post-hoc pairwise analysis using Mann-Whitney U tests Bonferroni corrected for multiple comparisons. ^asignificant differences between healthy controls and PD patients H&Y III. ^bsignificant differences between PD patients H&Y I and III. ^csignificant differences between PD patients H&Y II and III.

DISCUSSION

In the present study, we demonstrated significant differences between PD patients and healthy controls in a global empathy score of the validated questionnaire IRI. To evaluate the nature of the detected differences, we further analyzed the subscales of the questionnaire as it includes both cognitive and affective aspects of empathy. The scales Empathic Concern and Personal Distress measure affective components of empathy because they are directed at typical emotional reactions triggered by experiencing other persons [15]. These reactions are either ‘self-oriented’ (e.g., anxiety, discomfort) as implemented in the subscale Personal Distress or ‘other-oriented’ (e.g., compassion, concern) as implemented in the subscale Empathic Concern [14]. In both subscales, we did not find significant differences between patients and controls, suggesting that PD patients do not have altered empathic abilities in terms of their emotional reactions. The scale Perspective Taking assesses the ability to adopt another’s point of view corresponding to the ToM concept. On this scale, PD patients showed significant lower scores than healthy controls. This finding is consistent with previous studies which demonstrated ToM deficits in PD patients [10, 11]. Fantasy measures the tendency to identify with fictitious characters. Although this scale is often classified as an affective empathy component, we are in accordance with de Corte et al. [30] of the opinion that it is difficult to characterise the Fantasy scale along the affective-cognitive dimension. We believe it includes both the cognitive adoption of another person’s point of view and resulting emotional reactions and therefore it can be classified as a mixed variable. In this study, PD patients scored significantly lower than healthy controls on this scale. Thereby, patients showed lower scores in the two subscales of the IRI that comprise cognitive empathy aspects. The other two subscales which are exclusively sensitive for affective components of empathy did not differ between both groups. These results indicate that lower empathy scores in PD patients are driven by a decrease in cognitive empathy aspects whereas PD patients do not have reduced empathic abilities in terms of their emotional reactions in interpersonal situations. In accordance with our results, Narme et al. [31] found a significant lower global empathy score in PD patients than in healthy controls using the IRI. However, they did not analyze the subscale results. Using another empathy measure (E-scale), Rosen et al. [32] did not find any differences in the cognitive or emotional sensitivity between PD patients and controls. This can probably be explained by the different instrument used and the smaller number of patients examined (20 PD patients vs. 75 PD patients in the present study).

Given the large number of patients included in our study, we were able to analyze empathy in relation to disease progression. Only patients in an advanced disease stage showed significant lower IRI scores whereas empathy was nearly unaffected in earlier stages of the disease. The correlation analysis showed an association between several empathy scores and disease duration supporting the relationship between empathic abilities and disease stage. However, the correlations were no longer significant after partialling out the l-dopa equivalent dose, and vice versa. These results indicate that a combined factor consisting of disease duration and stage as well as l-dopa dose has an impact on the empathy scores in PD patients. This factor can be summarized as “disease progression” in consideration of the fact that a longer disease duration is usually accompanied by a higher l-dopa dose and both variables are highly significantly correlated in our study sample, too (r = 0.659, p = 0.000). Our findings correspond to a meta-analysis from Bora et al. [33] which demonstrated that ToM deficits in PD patients are more severe in later stages of the disease. Not much is known about the networks for the emotional versus the cognitive components of empathy. Given the lack of affection of the affective but worse cognitive dimensions it is tempting to speculate that this might reflect an affection of the cognitive basal ganglia loop. Concerning the relationship between ToM deficits and executive functioning, previous studies showed heterogeneous results [34 –37]. In our investigation, we found only sporadic significant correlations between cognitive and empathy scores without a specific signature. However, most subjects in our study showed only slight cognitive impairments and a ceiling effect of cognitive measures might explain the absence of significant results. It should be noted that an exclusion of the depressed patients did not seem necessary given the fact that depression only correlated significantly with the Personal Distress scale which is not included in the global empathy score. Furthermore, this scale did not significantly differ between patients and controls.

There are few limitations of the study. First, empathy was solely assessed with a self-rating questionnaire. Therefore, the validity of our results must be confirmed on a behavioral level in future studies to clarify the impact of empathy deficits on patient’s social interaction and daily living. Second, most patients in the PD group were in mild to moderate disease stages. An analysis including patients in more advanced disease stages would be interesting to verify the stage dependent alterations of empathic abilities we demonstrated in our study. Third, there were differences between PD patients and healthy controls in terms of gender distribution. As this difference was not statistically significant, we do not assume a relevant effect on our results caused by this variable, however, it cannot be excluded with certainty.

In summary, this study showed reduced self-assessed empathic abilities of PD patients compared to healthy controls. The decrease is more pronounced in patient with advanced disease progression and is driven by alterations in cognitive empathy possibly related to the concept of ToM. The emotional aspect of empathy which includes an understanding and experiencing of other people’s emotions is not reduced even in advanced stages of the disease. We did not find evidence for an association between reduced empathy scores and neuropsychological functioning including measures for executive functions, memory, attention, visual-spatial abilities, and language.

CONFLICT OF INTEREST

The authors have no conflict of interest to report.

Footnotes

ACKNOWLEDGMENTS

For this study, part of the data was generated within the LANDSCAPE study. The LANDSCAPE study is part of the Competence Network Degenerative Dementias (KNDD) which was funded by the German Federal Ministry of Education and Research (project number 01GI1008C).

The supplementary material is available in the electronic version of this article: .

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