Key-words:
Clock drawing test - cognitive functions - Mini-Mental State Examination test - traumatic
brain injury
Introduction
Traumatic brain injuries (TBIs) are the leading cause of morbidity, mortality, disability
and socioeconomic losses globally, but of more concern in India and other developing
countries. It is estimated that nearly 1.5–2 million persons are injured and 1 million
succumb to death every year in India. Road traffic injuries are the leading cause
(60%) of TBIs followed by falls (20%–25%) and violence (10%). Apart from many other
causes of traumatic injuries, alcohol abuse/consumption is known to be present among
15%–20% of TBIs at the time of injury.[[1]] Subsequent to the brain injury resulting in trauma, cognitive deficits that can
follow TBI include impaired attention, disrupted insight, judgement and thought, reduced
processing speed, distractibility, and deficits in executive functions such as abstract
reasoning, planning problem, solving, and multitasking.[[2]] Memory loss, the most common cognitive impairment among head-injured people, occurs
in 20%–79% of people with closed head trauma, depending on severity.[[3]]
Clinically, cognitive impairment caused by TBI is different in mechanisms, clinical
manifestations, risk factors, and outcomes.[[4]] Therefore, it is necessary to establish a robust evaluation system exclusive for
post-TBI cognitive impairment because it may act as a decisive test for post-TBI cases
enabling them fit/unfit for public jobs/sensitive jobs and services. There are a number
of neuropsychological and extensive bedside tests available to evaluate executive
cognitive function, but most of them are time-consuming. The mini-mental status examination
(MMSE) and clock drawing test (CDT) are the two mostly adapted methods for cognitive
impairment screening.
The potential of CDT as a screening tool for cognitive impairment has long been a
matter of great interest. This is a cognitive test with a number of scoring variations,
most of which are fairly easy and simple to perform and assess.[[5]] Clock drawing involves comprehension, perception, memory, gross motor function,
visuospatial organization, concentration, numerical knowledge, concept of time, and
inhibition of distracting stimuli. Although it appears simple, drawing of a clock
correlates to a complex goal-directed behavior in an abstract environment.[[6]] It was originally used to assess visuo-constructive abilities, but abnormal clock
drawing occurs in other cognitive impairments also. The test can be performed on patients
who have verbal understanding, memory and spatially coded knowledge in addition to
constructive skills.[[7]] Education, age, and mood can influence the test results; subjects of low education,
advanced age, and depression performing more poorly.[[8]],[[9]]
Routine tests of cognition such as Mini-Mental State Examination (MMSE), developed
by Folstein, is a thirty-point questionnaire that is used extensively in clinical
and research setting to measure cognitive impairment.[[10]] It is also used to estimate the severity and progression of cognitive impairment
and to follow the course of cognitive changes in an individual over time, thus, making
it an effective way to document an individual's response to treatment.[[11]] At the same time, it often fails to identify executive dysfunction even if severe.
This study was undertaken to determine the uses and efficiency of CDT to identify
cognitive dysfunction and to assess its utility along with MMSE in identifying potential
executive cognitive dysfunction in the TBI patients during follow-up in a clinical
setting.[[12]],[[13]]
Materials and Methods
Patient selection
The study was carried out in the physiology department with the collaboration of the
neurosciences department at a tertiary level health-care facility of northern India.
A total of 134 patients were recruited for the study with effect from October 2018
to May 2019. These cases were treated previously at the health facility for TBIs and
were evaluated for cognitive functions during the follow-up, ranging from 3 weeks
to 6 months, in the out-patient department. All these cases were evaluated by a faculty
of Neurosurgery first and then were subjected for the cognitive battery of tests once
found suitable for these evaluations. Prior ethical clearance was obtained from the
institutional ethical clearance committee, and informed consent was taken from patients.
Cases who met the inclusion criteria were recruited in this study. Most of these were
admitted in the indoor patient department of neurosurgery department following TBI
and were discharged after their appropriate case management.
Inclusion and exclusion criteria
Cases in the age group of 18 years and above who were treated and discharged previously
from the health facility for TBIs and attending the out-patient department for follow-up
after a time-duration ranging from 3 weeks to 6 months, were included in the study.
Patients who had a history of any neurodegenerative illness, alcohol or substance
abuse, cognitive dysfunctions before the trauma, mental deterioration due to fulminant
infection or neurological disorders, patients with repeated trauma or any chronic
illness and uncooperative cases and those not providing their informed written consent
for participating in the study were excluded from the study. Illiterate patients who
were unable to follow verbal as well as written commands and those patients with altered
sensorium who could not be assessed by neurocognitive battery of tests were also excluded
from the study.
Battery of tests used for cognitive assessment
The Mini-mental state examination (MMSE) and CDT was used to measure cognitive impairment
in all TBI patients. The MMSE test, a thirty-point questionnaire, included questions
and problems of a number of higher mental skills like orientation, attention, calculation,
recall, language, repetition, and complex commands. On the other hand, the CDT was
a five points score scale which included questions related with the clock drawing
skills, namely, inclusion of every number, correct order of number, drawing correct
time, drawing of two clock hands, and correct numbers placed in the four quadrants
of the clock as CDT sub-tests. The subjects were presented with a white paper and
the instructions to draw a clock. There was no time limit. Free draw method was used
for CDT, in which subjects were instructed to draw a clock with the clock hands at
a fixed time, often ten past eleven.
Interpretations of MMSE and clock drawing test
For MMSE, any score of 24 or more (out of maximum 30) indicated a normal cognition,
while cognitive impairment categories and scores were mild (19–23 points), moderate
(10–18 points), and severe (≤9 points).[[14]] Even a maximum score of 30 points attained by a patient does not rule out cognitive
impairment as the presence of physical problems can also interfere with the interpretation
if not properly noted; for example, a patient may be physically unable to hear or
read instructions properly or may have a motor deficit that affects writing and drawing
skills, but his higher functions may be intact enabling the patients to perform the
cognitive functions efficiently.
For CDT, a total score of five was considered as normal cognition while test score
<5 pointed toward cognitive impairment.
The clinical and radiological assessment data were utilized for the categorization
of the type and site of TBIs which was collected from discharge summary and case files
of each patient in consultation with treating surgeons from the medical record department
of the university.
Statistical analysis
The data, thus collected, were analyzed using Statistical Product and Service Solutions
(spss software) IBM statistics, version 25, Chicago, USA. The association between
the presence of cognitive impairment and site of brain injuries by using both the
study tools (MMSE and CDT) was analyzed using Chi-square test, while ANOVA was used
to compare the mean scores of MMSE, CDT, Glasgow Coma Scale (GCS), and age. A value
of P < 0.05 was considered statistically significant.
Results
[[Table 1]] shows the association of various studied variables and the site of brain injury.
The site of injury was broadly categorized into frontal, temporal, parietal, occipital,
and multiple lobe injury/diffused axonal injury. Majority of TBI patients had frontal
lobe injury 50 (37.3%) and among them, most 40 (80.0%) were between 21 and 60 years
of age. Association between age and site of brain injury was not found to be statistically
significant (χ2 = 18.62, P = 0.098).{Table 1}
Table 1: Association of various variables and site of brain injury
Gender wise distribution showed that 86 (64.2%) males and 48 (35.8%) female as study
participants. Frontal lobe injury was predominant in both the gender with males accounting
for 29 (21.6%) and females accounting for 21 (15.2%). Association between gender and
site of injury was found statistically not significant (χ2 = 3.05, P = 0.550).
Although 102 (76.1%) of the patients were educated, only up to high school, the insignificant
association between the site of brain injury and educational status of patients (P
= 0.072) was observed.
According to GCS status, 106 (71.9%) patients had mild illness GCS (13–15) of which
majority 38 (28.4%) had frontal lobe injury followed by parietal lobe injury 22 (16.4%).
Association between the site of injury and GCS scale status was not statistically
significant (P = 0.326).
Based on scores obtained by patients in mini-mental score examination, it was observed
that 62 (46.3%) cases had normal cognitive functions while 38 (28.4%), 24 (17.9%),
10 (7.5%) had mild, moderate, and severe cognitive impairment, respectively. There
was a statistically significant association between the site of injury in patients
and the level of cognitive impairment based on MMSE score (P < 0.001). It can be fairly
predicted that the frontal lobe is the most common site for cognitive compromises.
[[Table 2]] depicts that there was a statistically significant association (P < 0.001) between
the cognitive status of patients on the basis of overall MMSE score and the site of
brain injury. 76 (56.7%) of the cases had cognitive impairment (MMSE score <24) with
majority 44 (32.8%) patients having frontal lobe injuries followed by 14 (10.1%) having
brain injuries in the temporal lobe. On evaluating the cognitive status and the site
of injury according to all the eight individual components of MMSE, it was observed
that orientation to time (χ2 = 40.7, P < 0.001), orientation to place (χ2 = 42.05,
P < 0.001), attention and calculation (χ2 = 42.03, P < 0.001), repetition of words
(χ2 = 17.3, P = 0.002), recall of words (χ2 = 11.81, P = 0.02), and complex command
(χ2 = 25.75, P < 0.001) were found to have statistically significant association between
them. Other components such as registration of words (χ2 = 4.99, P = 0.29) and language
(χ2 = 1.83, P = 0.767) were not significantly associated with brain injury site.{Table
2}
Table 2: Association between various components of mini mental state examination and site
of brain injury
[[Table 3]] depicts that there was statistically significant association (χ2 = 35.77, P < 0.001)
between the cognitive status of patients on the basis of overall CDT score and the
site of brain injury. It was observed that 102 (76.1%) of the cases had cognitive
impairment (CDT score <5) with the majority among them, 49 (36.6%) cases, having frontal
lobe injury followed by 19 (14.2%) having brain injury in the parietal lobe.{Table
3}
Table 3: Association between various components of clock drawing test and site of brain injury
On evaluating the cognitive status and the site of brain injury according to all the
five individual components of CDT, it was observed that inclusion of every number
in the clock (χ2 = 31.28 P < 0.001), correctly ordered number on the clock (χ2 = 46.21,
P < 0.001), drawing correct time on the clock (χ2 = 54.42, P < 0.001), correctly drawing
of two clock hands (χ2 = 38.86, P < 0.001), and correct number placed in the four
quadrants of the clock (χ2 = 36.01, P < 0.001) had statistically significant association
between them.
[[Table 4]] depicts that the mean age, mean MMSE score, CDT score of patients is significantly
associated with the site of brain injury and their P values are P = 0.047, P < 0.001,
P < 0.001, respectively, but mean GCS score is not significantly associated with the
site of injury (P = 0.26).{Table 4}
Table 4: Association of mean scores of age, Glasgow Coma Scale, mini-mental status examination
and clock drawing test and site of brain injury
[[Table 5]] reveals that according to the MMSE score results, 76 (56.7%) of the TBI patients
had cognitive impairment while CDT detected 102 (76.1%) as having cognitive impairment.
There was a statistically significant association between the cognition status and
test used for its detection (χ2 = 11.31, P = 0.001).{Table 5}
Table 5: Comparison between mini-mental status examination and clock drawing test results
for cognitive status of traumatic brain injurie patients
Discussion
The present study has revealed that older adults and middle-aged patients who met
with TBI (mainly frontal lobe injury) exhibited poor cognitive performance. Similar
observations were also reported by Gruber et al,.[[15]] Bruns and Hauser,[[16]] Paula et al.[[17]] and Crowe et al.[[18]] in their studies.
It was observed that the cognitive impairment detected by both MMSE and CDT tests
was mainly seen in the frontal lobe injury followed by parietal and temporal lobe
TBIs patients. Similar findings were reported by Gershberg and Shimamura,[[19]] in their study and discussed that cognitive impairment in these patients occurs
due to damage to prefrontal cortex which disrupts a variety of cognitive functions,
including planning, problem solving, and temporal organization.
On evaluating the cognitive status and the site of injury according to all the eight
individual components of MMSE, it was observed in the present study that orientation
to time, orientation to place, attention and calculation, repetition of words, recall
of words, and complex command were significantly associated with site of brain injury.
Patients with frontal lobe brain injury have reported highest risk of cognitive impairment
by both MMSE (32.8%) and CDT (36.6%) therefore verifying the role of frontal lobes
in cognitive function impairment. Few studies have also shown strong evidence that
frontal damage disrupts performance on the test of recognition and free recall.[[20]],[[21]]
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[[22]] and the content is highly verbal, lacking sufficient items to adequately measure
visuospatial and/or constructional praxis. Hence, its utility in detecting cognitive
impairment caused by focal lesions is uncertain. On the other hand, in drawing the
clock as done in CDT, different cortical systems work simultaneously, including the
frontal, parietal, and temporal lobes.[[23]],[[24]] Thus, different cognitive abilities can be measured, by CDT such as selective and
sustained attention, auditory comprehension, verbal working memory, numerical knowledge,
visual memory and reconstruction, visuospatial skills, on-demand motor execution (praxis),
and executive function. It is apparent from current study that parietal lobe dysfunctions
are mainly detected by CDT and not by MMSE. However, CDT detects frontal, parietal
dysfunctions and occipital lobe also, in contrary to MMSE which detects mainly frontal
and temporal dysfunctions.
It was observed in the present study that 10.1% of temporal lobe injury patient had
lower cognitive impairment by MMSE and by CDT score it was observed in 13.4% patients.
Findings of many researchers confirm that the temporal lobe plays a significant role
in both retrograde and anterograde memory as it is well-known for its function in
memory storage, language recognition, and processing of audio-visual sensory input.
The role of medial temporal lobes and hippocampus as memory center has been widely
described, and researches have shown that focal lesions in the hippocampus result
in limited impairment of memory function, whereas extensive lesions that include the
hippocampus and the medial temporal cortex result in severe impairment.[[21]],[[25]]
Another finding of the present study was that 7.5% of parietal lobe injury patients
have shown lower scores for MMSE <24 indicating cognitive disruption for orientation,
attention, repetition of words and complex command, while 14.2% of parietal lobe injury
patient had low CDT score <5 with cognitive function impairment in the inclusion of
every number on clock, correct order of number, drawing correct time, drawing of two
clock hands, and correct number placed in the four quadrants, as CDT subtests. Scientists
have found in their studies that parietal lobe injury is associated with verbal short-term
memory loss due to damage to the supramarginal gyrus. It usually includes right-left
confusion, difficulty with writing (agraphia) and difficulty with mathematics (acalculia),
language (aphasia) and the inability to perceive objects. Right side damage can also
cause difficulty in making things (constructional apraxia), denial of deficits (anosognosia),
and drawing ability.[[26]]
It was also noted that 7.2% of occipital lobe injury patients showed significantly
lower CDT score while they had normal MMSE score, thus focusing on the visual memory
disruption associated with the occipital lobe injury. Occipital lobe receives incoming
information, which is processed and immediately sent to the hippocampus, where it
is formed into short-term memory. Thus, hampering of visual perception due to occipital
brain injury leads to impairment of various subsets of CDT.
The results indicate that the ability to detect cognitive impairment of CDT in TBI
patients was better than MMSE and this difference was found to be statistically significant
(P = 0.001). In all the groups of TBI, it was seen that many patients had normal MMSE
scores and abnormal CDT scores; while, in contrast, it was very rare for patients
to have normal CDT score but abnormal MMSE score. When the MMSE score was abnormal
and suspicion of cognitive impairment was high, abnormal CDT reinforced the diagnosis
of cognitive impairment. MMSE mainly focused on recall, speech, orientation with less
focus on visuo-constructive function. In comparison, CDT had wider coverage and well
balanced with every subtest.
Conclusion
-
The CDT was able to access cognitive function disruption in those patients in whom
the mini mental score examination was not able to assess the same and this difference
in detection capabilities of both the tests was statistically found significant. The
study may help in fetching the practicability and preference of one of these two tests,
based on their merits, if any
-
CDT can detect the dysfunctions of frontal, parietal, temporal, and occipital lobes
in contrary to MMSE. However, this test cannot be used in illiterate subjects
-
CDT was found as a multidimensional test which covers visuospatial and visuo-constructive
skills, the symbolic and graphomotor representation, the auditory language skills,
attention, semantic memory, conceptual abilities, and the executive function, which
includes organization, planning, and parallel processing. On the other hand, MMSE
was found good in assessing attention, language, memory, orientation, and visuospatial
proficiency. It is clearly understood by using these two tools that some points of
cognition were covered by MMSE but CDT covered all the higher cognitive functions
-
It was concluded that CDT is better tool to assess cognitive impairment in TBI because
it is simple to perform and less time consuming, quick to apply, well accepted by
patients, easy to score and relatively independent of language, education, and culture
of the patients
-
MMSE detects mainly temporal and frontal dysfunctions, takes 30 min to perform test,
time-consuming and language is main hurdle while CDT is fast screening tool (takes
approximately 5 min), easy to administer, well tolerated, free of cost, may be useful
in developing countries.
