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The effects of cognitive rehabilitation on relapsing remitting multiple sclerosis patients.


Cognitive disorder is an important and common symptom in multiple sclerosis (MS) patients with effects on the quality of life, social life, and career (1,2). With reported prevalence of 43-70%, cognitive disorder is observed from the early stages of the disease and even in clinically isolated syndrome (3). Age, level of education, disease duration, course type, and disability level are parameters that are associated with cognitive disorders. Gender has been reported to be unrelated to cognitive functions. Data on Expanded Disability Status Scale (EDSS) to cognitive disorder relationship are unclear (4,5,6,7). Cognitive functions that are mostly affected in MS patients are information processing speed, visual learning, and long-term memory (8). Simple attention and basic verbal skills are usually maintained until the late phases (9). Reduced participation in social activities, higher unemployment rate, greater difficulty in performing routine housework, and consequently a higher risk of psychiatric disorders have been demonstrated for MS patients in parallel with cognitive effects (9).

The limits of pharmacologic therapy in the symptomatic treatment of MS-related cognitive disorders redirected the interest towards cognitive rehabilitation. Cognitive rehabilitation has been in use for years for treating cognitive disorders that are due to head trauma, stroke, and operated central nervous system tumors (10). Rehabilitative practices in the treatment of cognitive disorder in MS patients have recently gained popularity, with positive results being reported from an increasing number of studies (II). The studies performed include computer-aided systems, as well as home-based training programs, which may or may not include compact discs (CDs). Studies particularly on correcting attention, memory, and executive functions are more prevalent. Improvement was demonstrated mostly for learning and memory functions.

Experience related to cognitive rehabilitation for MS patients in Turkey is quite limited. The present study is one of the first and here, we have investigated the effects of an 8-week computer-aided cognitive rehabilitation application in RRMS patients.


Patients being followed-up and treated by the MS and Demyelinating Diseases Polyclinic of Bakirkoy Psychiatric Hospital were reviewed using Rao's BRB cognitive test battery and cognitive rehabilitation was recommended to patients who performed below 5 percentile in at least two tests.

Patients who provided informed consents were evaluated for inclusion in the study. Approval of the hospital's ethics board was granted for the study The inclusion criteria were confirmed as MS diagnosis as per the 2005 Revised McDonald criteria, relapsing remitting multiple sclerosis (RRMS) clinical form, patients of both sexes aged 18-45 years, ability to read and write, Expanded Disability Status Scale (EDSS) [less than or equal to]5.5, Beck Depression Scale score [less than or equal to]17, being episode-free or not having received steroid treatment for the past one month and absence of alcohol, substance and psychotropic drugs use for the past 3 months. The exclusion criteria were the presence of progressive (secondary progressive and primary progressive subtypes) multiple sclerosis, experiencing an attack or receiving steroid treatment over the past one month, presence of an acute psychiatric condition or a non-MS neurological condition that may affect the cognitive status, use of any drugs that may affect the cognitive status, EDSS >5.5, and Beck Depression Scale score >17. Thirty-two patients meeting the inclusion and exclusion criteria were included in the computer-aided cognitive rehabilitation program, which was supervised by an experienced clinical psychologist and lasted 1 h/week for 8 successive weeks between March 2010 and March 2011. The patients were assessed using the BRB cognitive battery before cognitive rehabilitation and at the end of weeks 4 and 8 to evaluate the effects of rehabilitation.

The following tests, in addition to the tests performed at baseline and at weeks 4 and 8, were also performed: paced auditory serial addition test (PASAT), Spatial Recall test I, Selective Reminding test, Spatial Recall test II, Symbol Digit Modalities test, Spatial Recall test III, and Verbal Fluency test. The tests and rehabilitation program were performed in a dedicated, quiet room, which was isolated from the external stimulants to the highest possible extent.

Rehabilitation exercises focused on attention, sustainable attention, information processing speed, and verbal and visual memory Visual pattern, letter, and digit recall studies were performed on the attention screen. Time management and math problem solving exercises were performed on the information processing speed screen. Memory exercise screen included object identifying, cause identifying, problem solving, and deduction exercises. Identifying antonyms and synonyms, word association, word recall, and sentence completion exercises were performed on the verbal memory screen. Visual image identification, image confirmation, and finding similar and dissimilar image exercises were conducted on the visual memory screen.

Expanded Disability Status Scale was used to evaluate clinical status. Beck Depression Inventory was performed for depression assessment for all patients. The patients' quality of life was evaluated with Functional Assessment of Multiple Sclerosis (FAMS). The patients' cognitive status was evaluated with Multiple Sclerosis Neuropsychological Questionnaire (MSNQ) patient form and Brief Repeatable Battery (BRB).

Beck Depression Inventory included four choices for each of the 21 symptom category. The patient is asked to select the sentence that best corresponds how he/she felt during the last week including the day the inventory was completed. Each item is given a score from 0 to 3. Scores 17 and above from this inventory is considered to indicate the presence of depression.

Functional Assessment of Multiple Sclerosis is a self-reported form commonly used to assess the quality of life in MS patients. FAMS contains six scales (mobility symptoms, emotional status, overall status, and familial/ social status). Forty-four of the 59 statements in total are used for scoring and the patient is expected to give a score from 0 to 4 based on how a statement corresponds to his/her condition (12).

The Multiple Sclerosis Neuropsychological Questionnaire screening test includes patient and caregiver forms. In this self-reported test of 15 questions, the responses are scored from 0 to 4 (13). MSNQ patient form was used in the present study and, based on the normative data obtained from healthy individuals in Turkey scores above 22 were considered to indicate pathology.

Brief Repeatable Battery is the most commonly used battery of neuropsychological test for cognitive status assessment in MS patients with high specificity and sensitivity It takes about 30 min to complete the tests. Previous studies have found a sensitivity of 71% and a specificity of 94% (14). It includes PASAT Selective Reminding test, Spatial Recall test, Symbol-Digit Modalities test, and Verbal Fluency tests (14,15).

Paced Auditory Serial Addition test (PASAT) has two forms and the subject is asked to sum up the last two numbers, which are uttered successively It assesses sustainable attention and information processing speed. A maximum of 60 correct responses may be given (16).

Selective Reminding test (SRT) assesses verbal learning and recalling. The rater reads the 12 words in the list and the patient is asked to remember these words and then repeat them. At the second attempt, the patient is told only the words he/she could not remember during the previous attempt and is asked to recite the complete list. This continues up to 6 attempts and the number of all words remembered at the sixth attempt is summed up (17).

In the Spatial Recall test (SPART), also known as the 10/36 test, the patient is asked to memorize the locations of 10 round marks placed in a checkerboard design of 6x6 squares and to remember them later Three learning attempts and delayed recall phase at 25 min are performed. Visuospatial learning and long-term memory are assessed (15).

In Symbol-Digit Modalities, the patient is given a key comprising symbols numbered from 1 to 9. A score is given for each correct matching in 90 s. The maximum score is 60. Attention, visual/spatial information processing speed, and working memory are assessed (18).

In the verbal fluency test, the patient is asked to say as many words as possible for 1 min. In the two alternative forms, the patient is asked to list fruits and vegetables in form A and animals in form B (18).

Statistical Analysis

Statistical analyses in this study were performed using Number Cruncher Statistical System (NCSS) 2007 Statistical Software (Utah, USA) package. Descriptive statistics (mean, standard deviation) as well as the following were used for data evaluation: one-way variance analysis for inter-group comparisons, Tukey multiple comparison test for subgroup comparisons, paired variance analysis for follow-up comparisons of groups, Newman Keuls multiple comparison test for subgroup comparisons, and Pearson correlation analysis to determine the inter-association of the data.


Thirty-two patients meeting the study criteria were studied during the study period.

Patients' ages ranged from 24 to 45 years, with a mean age [[+ or -]standard deviation (SD)] of 36.09 [+ or -] 7.19 years. Of the patients, 75% (n=24) were females and 25% (n=8) were males. The disease duration ranged from 1 to 24 years, with a mead duration ([+ or -]SD) of 9.31 [+ or -] 7.55 years (Table 1).

Of the patients, 46.88 (n= 1 5) were graduated from primary school, 43.75% (n= 14) from secondary or high school, and 9.37% (n=3) had university degree or above. FAMS scores ranged from 27 to 173, with a mean ([+ or -] SD) score of 69.5 [+ or -] 30.27. Beck Depression Inventory scores ranged from 4 to 17, with a mean ([+ or -] SD) score of 12.97 [+ or -] 3.81. EDSS scores ranged from 1 to 4, with a mean ([+ or -] SD) score of 2.08 [+ or -] 0.99.

Multiple Sclerosis Neuropsychological Screening Questionnaire, SPART I, SPART II, and SPART III tests did not differ significantly between baseline, follow-up 1, and follow 2 (p>0.05).

There was a significant difference in the scores of PASAT SRT I, SRT II, SDMT and WLG tests between baseline and follow-up 1 and follow-up 2 tests (p=0.000l). Advanced analysis demonstrated that the difference was originating from the baseline test results, where the values were significantly low, and that there was a significant increase in the results of tests 1 and 2 performed during the rehabilitation.

No significant relationship was observed between age and improvements in PASAT SPART I, SPART II, WLG, SDMT SRT I, or SRT II (p>0.05).

The mean scores of primary school, secondary/high school, and university groups from PASAT SPART I, SPART II, SPART III, WLG, SRT I, and SRT II were not significantly different (p>0.05).

The mean SDMT scores of primary school, secondary/high school, and university groups were statistically significantly different (p=0.042).

In conclusion, there was a marked improvement with cognitive rehabilitation in maintaining attention, working memory and information processing speed, verbal fluency, and verbal learning whereas there was no impact on visuospatial learning visuospatial (Table 2).


Cognitive effects have a direct impact on the daily life activities of MS patients (19). The quality of life of these patients is correlated with physical disability, psychiatric symptoms, disease duration as well as cognitive functions. There has been an increase in the number of the studies investigating the ways to correct or prevent cognitive disorder, which is of such vital importance for and common among these patients.

Although there are some studies on the effects of the attempted pharmacological treatments on cognitive impairment in MS patients, conclusive data is currently unavailable (20). It has been demonstrated that disease-modifying drugs reduce the inflammatory process and may protect against the development of new brain lesions and progressive brain atrophy and that they may thus be beneficial from the cognitive perspective in MS patients (21).

Several pharmacological agents such as cholinesterase inhibitors and memantine were tried in the treatment of cognitive disorder in MS but the results have not been satisfactory (22,23,24). In a study by Krupp et al. (23), donepezil, an acetylcholinesterase inhibitor resulted in significant improvement in verbal learning and memory tests and some improvement in attention tests, although the studies are inadequate (23). A 36-week, randomized, double-blind, placebo-controlled study with a 12-week follow-up period with rivastigmine, another acetylcholinesterase inhibitor has, likewise, unclear results (24).

Having drawn recent attention, rehabilitation programs' efficacy was demonstrated in several studies (11). Although cognitive rehabilitation studies performed for cognitive disorder that developed following brain damage such as head trauma and stroke achieved A, B, and C level of evidence, there is a need for studies that are well-designed in terms of patient selection and treatment standardization (10). Available studies on MS examined rehabilitations for the correction of attention, memory and executive function in particular. Learning and memory functions were those in which best recovery was achieved. The intention is to increase patients' cognitive performance with the help of certain techniques (association, positioning) given as part of rehabilitation (25).

Of the patients included in our study 75% (n=24) were females and 25% (n=8) were males, which was not consistent with literature data (26,27). This could be explained by the fact that there was a limited number of subjects in the study, that the study required continued participation, and that male patients failed to maintain participation due to their occupations. Patients' ages ranged from 24 and 45 years and the mean age was 36.09+7.2 years. There was no significant relationship between patient age and level of improvements in cognitive tests.

Mean scores from the tests excluding SDMT did not differ statistically significantly by patients' education levels in this study These results are not consistent with the relevant literature and this was attributed to the difference in the number of subjects in the two groups and absence of a control group (28). In a study by Tesar et al. (29), the two groups were comparable with regards to clinical and sociodemographic data and basic intelligence level.

There was no statistically significant difference between the patients' disease duration and tests. In a study by Brenk et al. (30), patients with a disease history of 3-10 years were included and comparable results were obtained.

Seven patients with Beck depression above 17 were excluded. Whether these patients had cognitive disorder accompanying depression is unknown and how cognitive disorder accompanying depression would respond to rehabilitation could not be determined. Patients with all degrees of cognitive impairment based on the BRB-N score were included in the study. However among patients diagnosed with severe depression, a group of patients i.e., those for whom severe cognitive involvement was identified might have not been included in the study. Thus, response to cognitive rehabilitation could not be assessed in these patients.

Multiple Sclerosis Neuropsychological Questionnaire data were obtained from the forms completed by the patients themselves in this study. No statistically significant differences were observed between baseline and first and second follow-up tests. Self-reported cognitive deterioration has been identified not to be a sensitive indicator of actual deterioration (31). Although MSNQ is an effective and useful screening test in identifying cognitive disorder, it does not provide as detailed information on the type of the cognitive disorder as BRB-N. In this study follow-up of patients who were evaluated with MSNQ and BRB-N and who were identified to have cognitive disorder were performed with BRB-N but correlations between the two tests were not studied. Previous studies indicate that MSNQ and BRB-N scores are independent (32,33).

Paced Auditory Serial Addition Test values at baseline and first and second follow-ups were not statistically significantly different. These results indicated that the cognitive rehabilitation given was quite effective on sustainable attention, working memory and information processing speed. Measuring attention, working memory, information processing speed, and SDMT was similarly significantly different between baseline and first and second follow-ups. Previous studies have likewise determined a marked improvement in PASAT and SDMT values following cognitive rehabilitation (11,29,34,35,36).

Although a favorable effect of cognitive rehabilitation on visual memory was demonstrated in a study by Shatil et al. (37), confirmed data regarding visuospatial learning and long-term memory from other studies are lacking. There were statistically significant in differences in SPART I, SPART II, and SPART III at baseline and in the first and second follow-ups. This may be attributed to the short rehabilitation duration and limited number of weekly sessions.

The impact of cognitive programs on verbal learning and verbal memory was demonstrated clearly in a study by Hildebrant et al. (34). Our study also demonstrated a statistically significant difference in SRT 1 values between baseline and first and second follow-ups. There was also a statistically significant difference in SRT 2 values between baseline and first and second follow-ups. Based on these results, cognitive rehabilitation was effective on verbal fluency and verbal learning.

Some of the studies involved computer-aided programs while others involved home-based training programs with or without CDs (11,29,30,35,36,37). The present study used a computer-aided rehabilitation program focusing on attention and memory functions. Favorable effects were identified with cognitive tests as a result of rehabilitation utilizing both methods.

Positive aspects of the present study were the use of BRB-N, which demonstrates the degree of cognitive impairment with very high sensitivity and specificity in MS patients and the detailed assessment of patients' depression status, quality of life, and functionality level. This was one of the first studies to use the Neurosoft software developed for the implementation of cognitive rehabilitation programs conducted for slowing down the loss of cognitive losses, which is common among MS patients, and developing strategies and achieving regeneration where possible, to correct and prevent cognitive impairment in the Turkish patient population.

The method to rule out the learning effect, which is one of the key aspects of cognitive tests, involving duplicate testing before starting rehabilitation and to document the second test was not used in this study. Instead, an attempt was made to exclude this effect by performing the tests, which comprise A and B forms, by using different forms for each occasion. The absence of a control group was one of the most important limitations of the study. Despite the negative aspects of the study including the limited number of subjects and short follow-up duration, the obtained data were substantially consistent with previous reports (Table 3).

In conclusion, it is important to identify cognitive impairment, which is common in MS patients and has substantial negative effect on the quality of life, and to implement curative or inhibitory therapeutic measures at the earlier phases before the patient's status gets more complicated. Cognitive rehabilitation programs are promising in this respect. Comprehensive studies with larger samples and longer follow-up durations supported by radiological data examining this significant problem in MS patients in the Turkish population are needed.

DOI: 10.5152/npa.2015.7425

Acknowledgements: Many thanks to psychologist Pinar Kaya and psychologist Elif Kurt for their support at the phase of rehabilitation process.

Conflict of Interest: No conflict of interest was declared by the authors.

Financial Disclosure: The authors declared that this study has received no financial support.


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Ilknur GUCLU ALTUN [1], Dursun KIRBAS [2], Deniz Utku ALTUN [3], Aysun SOYSAL [4], Pakize Nevin SUTLAS [4], Demet YANDIM KUSCU [4], Neslihan BEHREM GAYIR [4], Ekim ARSLAN [5], Baris TOPCULAR [6]

[1] Clinic of Neurology, Sanliurfa Balikligol State Hospital, Sanliurfa, Turkey

[2] Istanbul University Forensic Medicine Institute, Istanbul, Turkey

[3] Sanliurfa Public Health Management, Sanliurfa, Turkey

[4] 3th Clinic of Neurology, Bakirkoy Prof. Dr. Mazhar Osman Psychiatric Training and Research Hospital, Istanbul, Turkey

[5] 2th Clinic of Neurology, Bakirkoy Prof. Dr Mazhar Osman Psychiatric Training and Research Hospital, Istanbul, Turkey

[6] Clinic of Neurology, Istanbul Bilim University, Istanbul, Turkey

Correspondence Address: Dr. Dursun Kirbas, Istanbul University Forensic Medicine Institute, Istanbul, Turkey Phone: +90 532 235 23 59 E-mail:

Received: 19.09.2013 Accepted: 14.04.2014
Table 1. Distribution of age and disease duration by gender
(percentage, mean, standard deviation)

Gender distribution   Age                     Disease duration

         n     % *    Mean    SD ([+ or -])   Mean   SD ([+ or -])

Female   24   75.0    35.58       7.35        9.70       7.29
Male     8    25.0    37.62       6.92        8.12       8.70
Total    32   100.0   36.09       7.19        9.31       7.55

* Column percentage used. SD: standard deviation

Table 2. Mean scores, standard deviations, and extreme
values from the cognitive tests

            Test 1 results pre-rehabilitation

                Mean [+ or -] SD       Min   Max

MSNQ          19.97 [+ or -] 8.49       0    40
PASAT       29.21 [+ or -] 17.97 ***    0    56
SPART I        4.72 [+ or -] 2.02       1     9
SPART II       5.63 [+ or -] 2.09       2    10
SPART III      5.94 [+ or -] 2.54       1    10
SRT I        8.03 [+ or -] 2.36 ***     3    12
SRT II       6.72 [+ or -] 2.74 ***     0    11
SDMT        40.44 [+ or -] 17.04 ***    0    69
WLG         32.88 [+ or -] 9.87 ***     8    52

            Test 2 results at the end of week 4

                Mean [+ or -] SD       Min   Max

MSNQ          19.63 [+ or -] 8.29       3    39
PASAT       38.96 [+ or -] 16.84 ***    0    60
SPART I        4.31 [+ or -] 1.80       0     9
SPART II       5.28 [+ or -] 2.05       2    10
SPART III      5.53 [+ or -] 2.09       1    10
SRT I          9.59 [+ or -] 2.05       5    13
SRT II         7.91 [+ or -] 2.60       2    12
SDMT          46.41 [+ or -] 17.26     18    82
WLG          37.31 [+ or -] 1 1.13     14    59

            Test 3 results at the end of week 8

                Mean [+ or -] SD       Min   Max    p *      p **

MSNQ          17.34 [+ or -] 7.75       3    31    >0.05      --
PASAT       42.43 [+ or -] 15.43 ***    4    60    0.0001   0.0001
SPART I        4.22 [+ or -] 1.74       0     8    >0.05      --
SPART II        5 [+ or -] 1.80         2    10    >0.05      --
SPART III      5.16 [+ or -] 2.23       1    10    >0.05      --
SRT I         10.09 [+ or -] 1.77       6    13    0.0001   0.0001
SRT II          9 [+ or -] 2.29         2    12    0.0001   0.003
SDMT          46.47 [+ or -] 17.94     19    82    0.001    0.003
WLG           40.44 [+ or -] 9.95      19    60    0.0001   0.047

Statistical significance was set at p<0.05.

* One-way variance analysis for inter-group comparisons

** Tukey multiple comparison test for subgroup comparisons

*** Group causing significant difference

SD: standard deviation; Max: maximum; MSNQ: Multiple Sclerosis
Neuropsychological Questionnaire; PASAT: Paced Auditory Serial
Addition Test; SPART I: Spatial Recall Test I; SPART II: Spatial
Recall Test II; SPART III: Spatial Recall Test III; SRT I:
Selective Reminding Test I; SRT II: Selective Reminding Test
II; SDMT: Symbol Digit Modalities Test; WLG: Word Fluency Test

Table 3. Assessment of the cognitive
rehabilitation study

Study name                Number of subjects   Rehabilitation
                          in the patient       Method in the
                          and/or control       study

Tesar et al. (29)         19 (patient +        Computer aided

Brenk et al. (30)         27 patients          House-based
                          14 controls          training program

Mattioli et al. (35) *    20 patients          Computer aided

Hildebrandt et al. (34)   17 patients          Computer aided
                          25 controls

Shatil et al. (37)        59 patients          House-based
                          48 controls          training program

Chiaravalloti             29 (patients +       House-based
et al. (11) **            controls)            training program

Lincoln et al. (28)       240 (patients +      House-based
                          controls)            training program

Solari et al. (36) *      82                   Computer aided

Present study             32                   Computer aided

Study name                Duration and     Study results
                          frequency of
                          in the study

Tesar et al. (29)         4 weeks 3        Marked improvement
                          times/week       in executive
                                           functions, verbal
                                           learning and memory,

Brenk et al. (30)         6 weeks 1        Marked improvement
                          or 5 times/      in memory, working
                          week             memory and attention

Mattioli et al. (35) *    3 months         Improvement in
                                           processing speed and
                                           executive functions

Hildebrandt et al. (34)   6 weeks 5        Marked improvement
                          times/week       in verbal learning,
                                           verbal memory and
                                           working memory

Shatil et al. (37)        12 weeks 3       Improvement in
                          times/week       memory, verbal and
                                           visual memory

Chiaravalloti             8 sessions       Positive effect on
et al. (11) **                             learning and memory

Lincoln et al. (28)       4-8 months       No marked change

Solari et al. (36) *      8 weeks 2        Improvement in BRB-N
                          times/week       of at least 20% in
                                           at least 2 tests,
                                           improvement in word

Present study             8 weeks 1        Marked improvement
                          times/week       in attention,
                                           processing speed,
                                           working memory and
                                           verbal memory

* double-blind, randomized, controlled. ** randomized, controlled
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Title Annotation:Research Article
Author:Altun, Ilknur Guclu; Kirbas, Dursun; Altun, Deniz Utku; Soysal, Aysun; Sutlas, Pakize Nevin; Kuscu,
Publication:Archives of Neuropsychiatry
Article Type:Report
Date:Jun 1, 2015
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