Abstract
Purpose
To investigate the profiles of cognitive impairment through Montreal Cognitive Assessment (MoCA) and Mini-Mental State Examination (MMSE) in patients with chronic traumatic brain injury (TBI) or stroke and to evaluate the sensitivity of the two scales in patients with TBI.
Methods
In this cohort study, a total of 230 patients were evaluated, including TBI group (n = 103) and stroke group (n = 127). The cognitive functions of two groups were evaluated by designated specialists using MoCA (Beijing version) and MMSE (Chinese version).
Results
Compared with the patients with stroke, the patients with TBI received significantly lower score in orientation subtest and recall subtest in both tests. MoCA abnormal rates in the TBI group and stroke group were 94.17% and 86.61% respectively, while MMSE abnormal rates were 69.90% and 57.48%, respectively. In the TBI group, 87.10% patients with normal MMSE score had abnormal MoCA score and in the stroke group, about 70.37% patients with normal MMSE score had abnormal MoCA score. The diagnostic consistency of two scales in the TBI group and the stroke group were 72% and 69%, respectively.
Conclusion
In our rehabilitation center, patients with TBI may have more extensive and severe cognitive impairments than patients with stroke, prominently in orientation and recall domain. In screening post-TBI cognitive impairment, MoCA tends to be more sensitive than MMSE.
Keywords: Montreal Cognitive Assessment, Mini-Mental State Examination, Cognitive impairment, Cognitive assessment, Brain injuries, Stroke
Introduction
The high incidence of traumatic brain injury (TBI) in China is a result of rapid development in transportation and construction industry over the past decades. The epidemiology study showed that 60–70 people in every 100,000 in China suffered from TBI. One million additional TBI victims are estimated every year nationwide,1, 2 and tremendous economic and social resources are consumed, so the disease was regarded as “the silent epidemics” in last century. Cognitive impairment perhaps one of the most important factors influencing the rehabilitation outcome, is commonly observed in TBI survivors.3 Effective cognitive rehabilitation is vital for better recovery and depends on targeted cognitive treatment which demands good evaluation. However, TBI rehabilitation in China now is at an early development stage and there is no specific rehabilitation system for the post-TBI cognitive impairment. Most patients with TBI still receive the same cognitive evaluation and rehabilitation as patients with stroke. Clinically, cognitive impairment caused by TBI and stroke is different in mechanisms, clinical manifestations, risk factors and outcomes.4 Compared with patients with stroke, patients with TBI are younger and have a longer recovery that indicates a better rehabilitation outcome.5 Therefore, it is necessary and urgent to establish the evaluation and rehabilitation system exclusive to post-TBI cognitive impairment. Up to date, there have been a few large clinical researches focusing on TBI cognitive impairment evaluation.
The Mini-Mental State Examination (MMSE) and Montreal Cognitive Assessment (MoCA) are the two mostly adapted methods for cognitive impairment screening,6, 7 both of which have a Chinese version and their reliability and validity have been tested in previous studies.8, 9 Despite the common advantages such as simple application, exclusive coverage of cognitive domains and broad clinical application, two scales differ largely in their contents: MMSE emphasizes evaluation of speech and orientation while MoCA covers more cognitive domains, focusing on executive and visuoconstructive functions.7, 10, 11, 12 In comparison to MMSE, MoCA is better in the screening of mild cognitive impairments. It was reported that MoCA was better in sensitivity than MMSE when applied to the screening of mild cognitive impairments in diseases such as Alzheimer,13 stroke14, 15, 16 and Parkinson.17, 18 Although two scales have been introduced in cognitive evaluation of patients with TBI, the differences in their sensitivity and specificity are not clear. Which evaluation tool better fits stroke cognitive impairment for patients with TBI warrants further investigation. To address the above questions, we utilize both MMSE and MoCA to evaluate the cognitive impairment of both patients with TBI and with stroke. The differentiating cognitive profiles of TBI and stroke were explored to observe the sensitivities and advantages of MMSE and MoCA applied in TBI group. Our study may provide help in selecting a suitable tool for evaluating post-TBI cognitive impairment.
Materials and method
Patient selection
All procedures were in accordance with China Rehabilitation Research Center welfare guidelines and the study was approved by the Institutional Ethics Committee of China Rehabilitation Research Center. The participants gave their verbal informed consent, because they were only given MMSE and MoCA tests without any interventions. The participant consents were recorded by video, and the consent procedure was approved by the ethics committee. Patients admitted to our center for stroke (ischemia or hemorrhage) or TBI from January to December in 2012 were included. The stroke was diagnosed by the criteria of American Heart Association and TBI by the criteria of the American Congress of Rehabilitation Medicine. All patients suffered from first-ever stroke or TBI for 1–12 months.
Exclusive criteria included illiteracy, alcoholic or drug abuse, previous history of Alzheimer disease, Parkinson disease, degenerative diseases of nervous system or incapability of completing cognitive test for any conditions, such as conscious disorder, severe neuropsychological disorder, severe dysphasia, motor dysfunction of dominant hand and handicap of hearing or vision.
Data addressing
The baseline data of all participants such as sex, age of onset, educational level, medical history, region of lesion, etc were recorded in detail. Magnetic resonance imaging was performed for all patients.
Evaluation method
All patients were evaluated in awake and peace state by designated experts using MoCA (Beijing version) and MMSE (simplified Chinese version). Patients were randomized into two groups by selecting a number. Patients with odd number received tests in sequence of MMSE-MoCA, which was opposite for patients with even number. There was a 24 h interval between the two tests. A cutoff score of ≥27 on the MMSE was chosen to indicate normal cognitive function,10, 19 and a cutoff score of <26 on the MoCA was taken to indicate cognitive impairment (an additional point being added to the total score for patients with less than 12 years of education), according to the recommendation from published references.7, 15, 16
Statistical analyses
Comparisons between MMSE and MoCA subtest scores across memory in TBI and stroke groups were performed using ANOVA adjusted for age and education and pairwise comparisons with Student's t test for continuous variables and X2 for categorical variables. Enumeration data were presented as absolute value and percentage, while measurement data were expressed as the mean ± SD. X2 test and t test were performed to evaluate the significance of the difference between two groups. SPSS 16.0 software (SPSS, Chicago, IL, USA) was used. A value of p < 0.05 was considered statistically different and p < 0.01 was considered statistically significantly different.
Results
Baseline data of patients
A total of 230 patients (103 with TBI, 127 with stroke) were included in our study. Their baseline data were showed in Table 1. There was no difference in education level between two groups (p > 0.05). There was statistically difference in sex distribution (p < 0.05) and significantly different in onset age (p < 0.01) between two groups. More males were included in TBI group (TBI vs. stroke: 84.47% vs. 73.23%). Onset age was younger in TBI group (TBI vs. stroke: 35.9 ± 13.08 years vs. 53.87 ± 13.18 years). More bilateral frontal, temporal and diffusive lesions were observed in patients with TBI. Unilateral lesions, most in basal ganglia region, were observed more frequently in patients with stroke. There was no difference between two groups in parietal lesions.
Table 1.
The comparison of baseline data between two groups.
| TBI (n = 103) | Stroke (n = 127) | p value | |
|---|---|---|---|
| Male (n, %) | 87 (84.47%) | 93 (73.23%) | 0.040 |
| Onset age (means ± SD) years | 35.9 ± 13.08 | 53.87 ± 13.18 | <0.01 |
| Educational level P50 (P25, P75) | 9 (9,16) | 9 (9,16) | 0.696 |
| Years | |||
| Education ≤ 12 years (%) | 66 (64.08%) | 80 (62.99%) | 0.865 |
| Inflicted side (n, %) | |||
| Left | 21 (20.39%) | 44 (34.65%) | <0.01 |
| Right | 25 (24.27%) | 73 (57.48%) | <0.01 |
| Bilateral | 57 (55.34%) | 10 (7.87%) | <0.01 |
| Affected area | |||
| Frontal lobe | 31 (30.10%) | 18 (14.17%) | <0.01 |
| Temporal lobe | 36 (34.95%) | 21 (16.54%) | <0.01 |
| Parietal lobe | 20 (19.42%) | 19 (14.96%) | 0.371 |
| Basal ganglion | 17 (16.50%) | 94 (74.02%) | <0.01 |
| Diffusive | 39 (37.86%) | 3 (2.36%) | <0.01 |
| Two or more areas | 68 (66.02%) | 43 (33.86%) | 0.017 |
Comparisons of total scores and subtests scores in both groups
Table 2 indicates that, in both tests, total score of TBI group was significantly lower than that of stroke group, while there was significant difference in subtests score of orientation and recall between the two groups.
Table 2.
Comparisons of total scores and subtests scores between MMSE and MoCA.
| TBI (n = 103) | Stroke (n = 127) | t value | p value | |
|---|---|---|---|---|
| MMSE | ||||
| Total/30 | 18.63 ± 8.93 | 22.16 ± 7.75 | 3.157 | 0.001 |
| Orientation/10 | 5.76 ± 3.52 | 7.63 ± 3.18 | 4.234 | <0.001 |
| Registration/3 | 2.50 ± 1.01 | 2.69 ± 0.78 | 0.632 | 0.055 |
| Calculation/5 | 2.67 ± 1.96 | 2.85 ± 1.92 | 0.704 | 0.509 |
| Recall/3 | 1.50 ± 1.21 | 1.90 ± 1.13 | 2.606 | 0.012 |
| Naming/2 | 1.77 ± 0.63 | 1.84 ± 0.51 | 0.983 | 0.413 |
| Repetition/1 | 0.72 ± 0.45 | 0.80 ± 0.40 | 1.489 | 0.133 |
| Comprehension/3 | 2.17 ± 1.11 | 2.35 ± 0.98 | 1.304 | 0.213 |
| Reading/1 | 0.77 ± 0.42 | 0.85 ± 0.36 | 1.587 | 0.107 |
| Writing/1 | 0.55 ± 0.50 | 0.62 ± 0.49 | 1.051 | 0.293 |
| Drawing/1 | 0.52 ± 0.50 | 0.61 ± 0.49 | 1.367 | 0.171 |
| MoCA | ||||
| Total/30 | 14.84 ± 6.70 | 17.43 ± 7.23 | 3.157 | 0.007 |
| Visuoexecutive/5 | 2.18 ± 1.53 | 2.54 ± 1.63 | 4.234 | 0.106 |
| Naming/3 | 1.92 ± 1.17 | 2.21 ± 0.97 | 0.632 | 0.092 |
| Digit span/2 | 1.49 ± 0.68 | 1.50 ± 0.65 | 0.704 | 0.920 |
| Attention/1 | 0.50 ± 0.50 | 0.57 ± 0.50 | 2.606 | 0.291 |
| Calculation/3 | 2.04 ± 1.18 | 2.16 ± 1.05 | 0.983 | 0.621 |
| Repetition/2 | 0.71 ± 0.72 | 0.85 ± 0.78 | 1.489 | 0.178 |
| Verbal fluency/1 | 0.43 ± 0.50 | 0.54 ± 0.50 | 1.304 | 0.080 |
| Abstraction/2 | 0.58 ± 0.69 | 0.73 ± 0.81 | 1.587 | 0.221 |
| Recall/5 | 0.81 ± 1.36 | 1.35 ± 1.73 | 1.051 | 0.020 |
| Orientation/6 | 3.83 ± 1.91 | 4.51 ± 1.73 | 1.367 | 0.003 |
Distribution of MMSE and MoCA scores in both groups
Shown in Table 3, the sensitivity of MMSE to TBI was 69.90% while MoCA was 94.17%. The consistency test of two scales showed: Kappa value was 0.1314 with 95% CI (−0.0258, 0.2887). The sensitivity of MMSE to stroke was 57.48% while MoCA was 86.61%. The consistency test of two scales showed: Kappa value was 0.3103 with 95% CI (0.1749, 0.4456). In TBI group, 27 of 31 patients with normal MMSE score had abnormal MoCA score (MoCA < 26); in the stroke group, 38 of 54 patients (about 70.37%) with normal MMSE score had abnormal MoCA score (MoCA < 26).
Table 3.
Comparisons between MMSE and traumatic brain injury (TBI) for cognitive profile between TBI and stroke.
| MMSE < 27 | MMSE ≥ 27 | Total | |
|---|---|---|---|
| TBI | |||
| MoCA < 26 | 70 (67.96%) | 27a (26.21%) | 97 (94.17%) |
| MoCA ≥ 26 | 2 (1.94%) | 4 (3.89%) | 6 (5.83%) |
| Total | 72 (69.90%) | 31 (30.10%) | 103 (100%) |
| Stroke | |||
| MoCA < 26 | 72 (56.69%) | 38a (29.92%) | 110 (86.61%) |
| MoCA ≥ 26 | 1 (0.79%) | 16 (12.60) | 17 (13.39%) |
| Total | 73 (57.48%) | 54 (42.52%) | 127 (100%) |
Patients with normal MMSE but low MoCA.
In the TBI group, only 4 patients had normal scores in MoCA and MMSE. Equally, 99 patients had abnormal scores in MoCA and/or MMSE. In the stroke group, 16 patients had normal scores of MoCA and MMSE; 111 patients had abnormal scores in MoCA and/or MMSE. The general sensitivity of two scales was 87.40%.
Discussion
Epidemiologically, TBI and stroke vary significantly in risk factors, onset age and injured regions. Large epidemiological studies have indicated that most TBI victims were the youth and middle-aged adults,20 while the peak onset age was old in patients with stroke.21 In our research, statistical analysis also showed that the onset age of patients with TBI was significantly younger than that of patients with stroke.
The results indicate that the sensitivity of MoCA in the TBI group is better than that of MMSE. In both groups, a large portion of patients had normal MMSE scores but abnormal MoCA scores. In contrast, it was rare for patients to have normal MoCA but abnormal MMSE scores. We saw the poor consistency of two scales in both groups, which was resulted from their different focuses. MMSE allocates 24/30 points to recall, speech and orientation but just 1/30 point to visuoconstructive function. In comparison, MoCA has a wider coverage and is well balanced with every subtest. The visuospace, attention and executive function are assigned more points (14/30). The patients with stroke or TBI with mild cognitive impairment performed poorly in executive, analysis and visuospace missions but relatively normally in recall, speech and orientation missions which can be identified easily with MMSE but generally evade the screen with MMSE. These results are consistent with the studies of Alzheimer's Disease, stroke, transient ischemic attack, Parkinson disease, etc.13, 14, 15, 16, 17, 18, 22
The comparison of MoCA and MMSE in both groups indicates that the total scores are significantly different and patients with TBI tend to have lower total scores in two tests. The subtest scores of MoCA and MMSE showed TBI group has significantly lower scores in orientation and memory than stroke group. The result indicates the higher susceptibility of orientation and memory in TBI in comparison with stroke. The MoCA subtests are not of equal difficulty. The 5-word recall item produced the most errors across both groups, and a ‘floor effect’ of this task has been noted in studies of more cognitively impaired patients making it a poor discriminator in such patients.
Despite the younger age of onset, the cognitive disorders of the TBI group are generally severer than that of stroke group. The comparison of MoCA and MMSE in both groups indicates that their total scores are significantly different and patients with TBI tend to have lower total scores in two tests. The subtest scores of MoCA and MMSE show that the TBI group has lower scores in all subtests than stroke group, significantly different in orientation and memory. The result indicates that post-TBI cognitive impairment is more extensive and severer, especially the orientation and recall which might be the important nature differentiating the cognitive stroke impairment. The severance and extensiveness of post-TBI cognitive impairment may be mainly associated with lesion region. The lesion regions of TBI and stroke are different depending on their distinct mechanisms. Cortical lesions of frontal and temporal lobe etc as well as bilateral and diffusive injuries are common in TBI group compared with stroke group, which may explain the severer and more extensive cognitive impairments of patients with TBI. Inflictions in stroke group are mainly in basal ganglion region and cause more limited and milder cognitive impairments.
The results showed that patients in both groups had relatively low scores in some MMSE and MoCA subtests: calculation, writing and drawing subtests for MMSE; registration, naming, repetition, comprehension and reading subtests for MoCA. However, there were no significant differences in these subtests between two groups. Therefore, characteristics of post-stroke and TBI cognitive impairments may be similar in some aspects. It has been confirmed that executive function and recall were the most susceptible cognitive domains in mild patients with TBI.4, 23, 24, 25 The impairments of information processing and executive function are prominent in post-stroke patients with mild cognitive impairment.26, 27, 28 Therefore, patients in both groups, especially those with moderate/severe cognitive impairment, had poor performance in subtests concerned with memory and executive function. No significant differences were found between two groups in subtests of attention, speech, abstract ability, calculation, executive function, etc. The exclusion of patients with severe dysphasia from our research may explain the insignificant difference in subtests concerned with speech. On the other hand, the weights of these subtests relative to total scores may be too small to present the differences fully.
Notably, patients in both groups have higher scores in MoCA in comparison with MMSE, mainly owing to their different emphasized domains. Due to the exclusion of patients with severe dysphasia, patients in two groups have relatively high scores in subtests concerned with speech. The weights of speech concerned subtests of MMSE are higher than those of MoCA (9/30 VS 3/30),6, 7 so patients have higher total score of MMSE than that of MoCA. The differentiations of subtests in two scales indicate that they are complementary and could be utilized combined in clinic to improve the identification of cognitive disorders significantly.
Patients in our research were recruited in rehabilitation center and most of them were severely injured in TBI or stroke. Therefore, the proportion of patients with moderate/severe was large and the sensitivity and differentiation of subtests of two scales may be affected. On the other hand, we excluded the patients incapable of cooperation for severe dysfunction of listening comprehension and oral expression.
Considering the percentage of speech evaluation in MMSE, the exclusion may influence the MMSE score. In addition, the similarities of two scales in some subtests content as well as the testing interval time and sequence may have affected the results.
Conclusion
Notably, impairments of cognition, especially orientation and recall function, may be severer and more extensive in TBI inpatients than stroke inpatients and thus demand the attention of clinicians. MoCA, as an easy-to-operated tool for cognitive impairment screen, can be used in TBI patients for its higher sensitivity. However, because two scales focus on different cognitive domains, we recommend combined application of both scales to optimize cognitive impairment screen and fully understand its characteristics. In the future, researches with large sample and follow up are needed to explore the differences between post-TBI and stroke cognitive impairments in influencing factors and effectiveness of rehabilitation.
Fund
This study was supported by the special basic research fund for Chinese central public research institutes (No. 2013CZ-30, 2013CZ-41).
Footnotes
Peer review under responsibility of Daping Hospital and the Research Institute of Surgery of the Third Military Medical University.
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