Social Cognition Impairments in Patients with Multiple Sclerosis: Comparison with Grade of Disability
Correspondence Address: Source of Support: None, Conflict of Interest: None DOI: 10.4103/0028-3886.279700
Source of Support: None, Conflict of Interest: None
Keywords: Expanded Disability Status Scale, grade of disability, multiple sclerosis, social cognitionKey Messages: Social cognitive impairments can manifest independently or in addition to physical deficits in MS and therefore the cognitive evaluation should be a part of general assessment and follow up in these subjects.
Multiple sclerosis (MS) is a chronic inflammatory autoimmune degenerative disease of the central nervous system (CNS) which disables patients both physically and neuropsychologically. The two types of impairment may occur either simultaneously or independently. Neuropsychological disturbances in MS were discovered and described as early as the 19th century by Charcot. However, these disturbances have been neglected both in clinical practice and research for many years. Currently, cognitive impairments in MS engage the attention of a growing number of scientists.,,
A less studied aspect of cognition is the so-called social cognition, which includes emotion perception from human faces, prosody, empathy, and theory of mind (ToM)., Most recent studies have established that important social cognitive skills are impaired in MS patients due to disorders in the left inferior frontal and medial frontal cortices. ToM is based on “reading the mind” of others through analyzing facial expression and other behavioral signs., In 2013, Mike et al. established that both dislocation mechanism due to lesions in the white matter and cortical thinning of specific brain areas could lead to cognitive deficits in MS patients, which affect emotion facial processing (the right and left fusiform face areas, the frontal eye fields, and the right entorhinal cortex zones) and mental state recognition based on facial expressions (the left temporal pole).
The impairment of social cognition skills makes social communication difficult and leads to inefficient social integration and individual isolation., For social cognitive impairments due to suspected anatomic-functional damage to be registered in MS patients, the development of these impairments during the course of the disease needs to be observed.
To examine the impairment of social cognition and its potential relationship with grade of disability in MS patients.
Our study included 17 healthy controls and 36 patients with clinically confirmed MS according to the revised McDonald Criteria from 2010. The sample included outpatients from Multiprofile Hospital for Active Treatment-National Heart Hospital and healthy controls (medical staff and relatives of patients treated in the healthcare institution). The patients were selected at random and were extracted from the hospital database.
According to inclusion criteria all the patients were diagnosed with relapsing-remittent MS, at 18–55 years of age, out of attack and in stable neurological condition for at least 30 days. The exclusion criteria required lack of severe depressive symptoms (score ≥29 according to Back Depression Inventory – second revision – BDI-II), pronounced cognitive decline (Mini Mental State Examination <24), head trauma, visual and/or auditory disturbances, history of alcohol and other substance abuse, premorbid learning difficulties and other significant medical conditions. Cognitive assessment was based on evaluation of: language skills (verbal fluency – two phonemic categories, each listed for 1 min), delayed recall (five items 10 min recall), visual spatial orientation (clock drawing test, drawing a cube), attention (Trial Making Test A—TMT-A) and speed of information processing/executive function (Trial Making Test B—TMT-B, Symbol Digit Modality Test written version – SDMT, Paced Auditory Serial Addition Test – PASAT 2''). The controls had not experienced any somatic and neurological disorders and had not searched help from psychiatrists, neurologists, or psychologists. Healthy controls were selected with demographics similar to those of the patients, including years of education, so that significant differences in results in this respect could be avoided [Table 1].
The tests were carried out with the informed consent of all participants in compliance with all ethical standards under the Declaration of Helsinki (1964 and subsequent revisions, including 15 April–15 June 2013). This study received approval from the local ethics committee.
To achieve the goal of the study, we invited both 30 patients with low grade disability and 30 patients with high grade disability to compare the results. Of them, a total of 41 people gave their informed consent. Five of the patients met the exclusion criteria, so they did not enter into the study. Clinical evaluation was made through Expanded Disability Status Scale (EDSS). Social cognition was assessed through a test battery selected by the research team:
Self-Compassion Scale, Neff (SCS) In this test the assessment of empathy was based on self-evaluation by giving a selective response to 26 questions, grouped into six categories (self-kindness, self-judgment, common humanity, isolation, mindfulness, and overidentified). The total score of the questionnaire is the sum of the sub-scores from the above mentioned sub-categories. The higher score corresponds to a high degree of empathy.
Reading the Mind in the Eyes Test (Baron-Cohen, S.) The “Reading the Mind in the Eyes,” based on interpretation of through nonverbal stimuli provides valuable information on the empathy. The task includes 36 pictures of eye pairs expressing feelings and thoughts. The subjects are asked to choose one of four options that in their opinion best describe the mental or emotional state of the person.
Theory of mind tests
Faux Pas Recognition Test (tests for interpreting information presented in an auditory manner) – the patients are asked to give relevant interpretation of four short situational stories perceived through listening. It is essential to differentiate a misleading moment included in the story and to give acceptable answers to the supplementary questions. For each correctly interpreted situation of auditory stories the subject receives 1 point. The presented situations are close to reality, i.e., might arise in everyday life.
ToM Cartoons – provides insight into the subject's ability to understand emotions and intentions, based on interpretation of cartoons. The task includes interpretation of two black and white cartoons which are stylized according to the requirements for neuropsychological tests and presented to the subjects for 30 s. Thus, minimal disruptions in social cognitive abilities can be detected. Before performing this test, the subject is instructed to carefully examine each of the cartoons and then give their most plausible interpretation. For each correctly interpreted cartoon 1 point is given.
Statistical analysis was performed with SPSS Statistics 20.0. Descriptive statistics, two-factor dispersion analysis for categorical data, Pearson's χ2 test, the exact test of Fisher, ANOVA (95% confidence interval) were used. The statistical significance was assessed through two-tailed tests and P< 0.05 was accepted as level of significance. InterCriteria Decision Making approach was applied due to relatively small groups to find intergroup and intragroup trends for the surveyed indicators.
The results obtained through social cognition tests on empathy for the three groups are presented in [Table 2].
No statistically important difference was found regarding Total Empathy Quotient between the three groups. However, there was a significant difference in the responses for two of the domains—self-kindness and self-judgment. The highest level of self-kindness was recorded in patients with a high degree of disability and the lowest in patients with low degree disability, which difference is statistically significant (P = 0.004). Regarding self-judgment, a regular tendency was found: the highest score was registered in healthy controls and the lowest in patients with EDSS ≥3.5. The difference between controls and each patient's group is statistically significant (P< 0.05).
Reading the Mind in the Eyes Test (visual empathy)
Concerning empathy assessed through Reading the Mind in the Eyes Test, a clear tendency was outlined for worsened results with increasing physical disability. A statistically significant difference (P = 0.0037) between the results of controls and those of patients with EDSS ≥3.5 was found.
Theory of mind
Faux Pas Recognition Test
The tests for interpreting stories perceived in an auditory manner (“faux pas”) showed a clear tendency toward “failure” among patients [Figure 1]. The healthy subjects comprehensively, correctly, and fully interpreted the presented situations and responded to the clarification questions. About two thirds dealt well with interpreting all four stories, and others with three of the four stories. The correct interpretation of all situations was rendered by half of the patients with a low grade of disability and only one third of the patients with a high grade of disability (P = 0.032). In our cohort, none of the subjects failed at all four tasks.
The results of interpreting ToM cartoons are presented in [Figure 2]. Both controls and patients with a low grade of disability showed similar results. Three fourths of the persons in each of these two groups gave complete and correct interpretations of the presented ToM cartoons. What makes the two groups different is that two of the patients with a low grade of disability (10%) failed at this test entirely. Regarding the group with a high grade of disability, only 33% of the patients completely coped with the test, 39% gave correct interpretation of one image, and 28% completely failed. The results of this group were statistically worse both in comparison to those of healthy controls and to those of patients with a low degree of disability (P = 0.0048).
Using InterCriteria analysis, we compared the results from social cognitive domains in pairs (all possible combinations: each person with each person) to find trends toward deterioration or improvement. We did not register relationships between the different domains, which correlates with the disease heterogeneity.
The results regarding social cognitive skills in MS patients were obtained under the following impaired cognitive domains compared to controls: verbal fluency (P< 0.05), five items 10 min recall (P< 0.001), visual spatial skills (P< 0.05), TMT-A (P< 0.001), TMT-B (P< 0.001), SDMT (P< 0.001), PASAT 2′′ (P< 0.001). We registered a clear trend for deterioration of basic cognitive domains with increasing of disability, but no statistically important difference was found between both patients' groups. No statistical significance regarding depression and anxiety was established.
The impairment of social cognitive skills deteriorates daily functioning in most subjects affected by MS. Thus, underestimation of the social cognitive status impedes complex evaluation of disability in patients with MS. Most studies devoted to neuropsychological impairments in patients with MS include cohorts in a relatively mild stage of the disease and with low EDSS scores. We have also included patients with high level of disability, and found that the grade of EDSS did not influence in the empathy quotient on the grounds of self-assessment in MS patients. These results replicate the conclusion obtained by Trevethan. At the same time, our study revealed that during deterioration of disability, patients tend to experience increased self-kindness. This seemingly paradoxical finding can be explained; it is logical for patients with worsening physical condition and decreasing self-judgment to place higher priority on kindness towards themselves. Our conclusion supports the supposition of E Rosti-Otajärvi and P Hämäläinen that it is possible to overestimate the frequency of neuropsychiatric symptoms in the early stages of the disease, especially when only self-assessment methods are used. On the other hand, when the disease progresses and self-judgment decreases, the prevalence of neuropsychiatric symptoms based on self-assessment could be underestimated. To avoid this subjectivity, we included additional measurement tools in the neuropsychological test battery: Reading the Mind in the Eyes test and ToM tests.
The results from the Reading the Mind in the Eyes test in our study showed, like other research,,, a gradual worsening of empathy during the progression of the disease. This claim is based on results obtained from studies using tests for facial expression detection in their neuropsychological batteries.In addition, we show that these impairments are reported in a stage of low grade of disability and progression in the course of the disease.
The level of social cognition in MS patients was first tested by Henry et al. Impairments are more prominent in emotion identification than in the identification of thoughts and intentions., In our study, ToM abilities evaluated through Faux Pas Recognition test and cartoons were significantly impaired in MS patients compared to healthy controls. In addition to Pöttgen et al., who established more pronounced disorder in ToM skills in the early stages of the disease, we registered deterioration of these impairments with the advancement of the disease.
As expected, the worsening of disability leads to an increased percentage of subjects misinterpreting a greater number of situations. In fact, failure to identify only one situation is not a reason to argue that the subject is experiencing a decline in social cognition, whereas failure to identify two or more situations can be interpreted as a real disorder impeding normal social functioning and daily activities. With progression of the disease and development of a high degree of disability, this problem affects an increasing number of patients and impaired social cognition is registered in twice as many patients with EDSS ≥3.5 as with a low degree of disability. Nevertheless, reported disorders are mild to moderate without encountering extremely severe impairment of social cognition. This provides reason for seeking an approach and areas for the integration and successful personal adjustment of these patients.
The manner of presenting information in ToM cartoons eliminates the hinting role of language. The results indicate that social cognitive skills are relatively preserved at the onset of disease. As the disease progresses in prevalence of EDSS ≥3.5, social cognitive skills assessed by ToM cartoons abruptly deteriorate. The results in [Figure 2] clearly show a tendency towards a decreased number of correctly interpreted situations with increasing grade of disability. Similar results have also been reported by other authors, but overall neuropsychological research in the field of nonverbal tests in patients with MS is still scarce.
Based on our results, the existence of a relationship between social cognitive decline and basic cognition in MS can be assumed. Furthermore, connections between impaired social cognition skills, depression and anxiety are unlikely. The above mentioned interactions are complex, still under investigation and the different authors “views[s] about them are contradictory.” But, due to their significant impact on neuropsychological status and quality of life in these patients, it is worthwhile to dedicate sufficient time and effort to perform more extensive research and monitoring over time.
Our study found that during the course of MS, deterioration of both social cognitive skills and basic cognitive abilities occurs which is parallel to physical disability. Difficulties in the correct identification of emotions, thoughts, and intentions in social situations could lead to interpersonal problems and can contribute to psychosocial dysfunction in MS patients. Therefore, social cognitive impairments are an essential aspect of general disability in these patients that may manifest independently or in addition to physical deficits. The early detection of such cognitive impairments as well as the search for and application of effective pharmacological and rehabilitative approaches should be among the main priorities in the care of these patients.
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Conflicts of interest
There are no conflicts of interest.
[Figure 1], [Figure 2]
[Table 1], [Table 2]