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ORIGINAL ARTICLE

Attention and executive functions in microsurgically

treated patients after subarachnoid hemorrhage
Maida Koso, Kemal Dizdarevic1
Department of Psychology, University of Sarajevo, Bosnia and Herzegovina, 1Department of Neurosurgery, Clinical Centre and
Medical School, University of Sarajevo, Bosnia and Herzegovina

ABSTRACT
Objectives: This research aimed to assess attention and executive functions in subarachnoid hemorrhage (SAH) patients.
Methods: The prospective, controlled, longitudinal study was conducted. There were two groups of patients (SAH and
lumbar microdiscectomy groups), and all of them were operated on by a single neurosurgeon (KD) in the same institution.
Preoperatively, SAH patients were in the Hunt‑Hess Grade I and II. They did not develop any focal neurological deficit or
hydrocephalus postoperatively. The patients were tested in 2‑time points: 15 and 45 days after microsurgery with a battery
of tests and questioners consisting of the Trail Making Test, the Sustained Attention to Response Task, the Hayling Sentence
Completion Test, The Attention/Concentration test of Attention, the Wechsler Adult Intelligence Scale (verbal part). Results
between groups were compared (sex, age; years of education and verbal IQ).
Results: It was found the presence of lower attention and executive function test scores in the SAH group of patients with
a trend of improving during the time.
Conclusion: The detailed neuropsychological assessment of operated patients who sustained SAH and were without the
focal neurological deficit postoperatively, showed declination in their attention and executive function with a trend of
cognitive recovery as time passes by.
Key words: Attention, executive functions, neuropsychological assessment, subarachnoid hemorrhage

Introduction options.[7] The study of Ropper and Zervas[8] pointed out that
25% of patients, year after successful treatment of ruptured
Cognitive dysfunctions after subarachnoid hemorrhage (SAH) intracranial aneurysm, have psychological and emotional
are well documented. Attention, memory and other cognitive deficits. The research of Ogden et al.[9] shows that the high
functions are very important for SAH patient rehabilitation percentage of patients demonstrated some mild to moderate
and their return to normal life. Numerous clinical studies psychosocial impairments. Hütter and Gilsbach[10] concluded
showed that cognitive deficits in these patients depend that a good neurological outcome does not exclude the
on a large number of factors, which includes the effects persisting neuropsychological deficits. Some other results
of hemorrhage and secondary brain ischemia, surgical [9, koso‑dizdarević] show that the severity of SAH is the most
performance,[1] timing of surgery,[2,3] anatomical location of important factor related to cognitive dysfunction. Hillis et al.[11]
the aneurysm,[4] family, friends and medical staff support,[5,6] examined patients with unruptured and ruptured aneurysm.
utilization of endovascular or microsurgical clipping Both groups performed significantly below published norms
on many of the neuropsychology tests after surgery. On the
Access this article online other hand, Otawara et  al.[12] found that microsurgery of
Quick Response Code: the unruptured intracranial aneurysm did not influence the
Website:
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cognition. Samra et al.[4] presented that cognitive improvement
that is present after 3 months, with a plateau between
9 and 15 months, was not affected by the location of the
DOI:
aneurysm. Many studies enrolled the patients with cognitive
10.4103/1793-5482.162683
impairment who harbored the anterior communicating
artery (ACoA) aneurysms.[13-15] However, cognitive results from
these studies were very similar with cognitive dysfunctions
Address for correspondence: found in the patients with aneurysm on other arteries. Lloyd
Asst. Prof. Maida Koso, Franje Rackog 1,
71000 Sarajevo, Bosnia and Herzegovina. et al.[7] examined the difference between cognitive function and
E-mail: [email protected] quality of life among patients treated by endovascular coiling

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Koso and Dizdarevic: Attention and executive function in SAH

and those treated by microsurgical clipping. The conclusion P  =  0.064) and with similar level of verbal intellectual
was that endovascular treatment and microsurgery had the skills measured with subtests Wechsler Adult Intelligence
similar impact on health-related quality of life and cognitive Scale  (WAIS)  –  comprehension  (ME  =  20,83, SDE  =  4,324;
function. Patients in both groups demonstrated a significant MK = 21,83, SDK = 4,726; t = −0.541, df = 22, P = 0.594) and
decline in cognitive function. The goal of the study that WAIS – Similarities (ME = 19, 08, SDE = 2,811; MK = 20,25,
conducted by Tuffiash et al.[15] was to identify changes in SDK = 3,079; t = −0.969, df = 22, P = 0.343).
cognitive function associated with surgical clipping of the
unruptured intracranial aneurysm. They found no evidence Following local Institutional Review Board/Ethics Committee
of subtle cognitive deficits resulting from aneurysm clipping approval, all subjects that match criteria during the
alone, suggesting that the common impairments after surgery 2 years of research were tested. They were all treated by
for ruptured aneurysms are due to SAH itself, complications a single neurosurgeon  (co‑author) at the Department of
of SAH such as vasospasm or hydrocephalus, or preoperative Neurosurgery, Clinical center University of Sarajevo. Criteria
stroke. Chan et al.[16] concluded that in patients with ACoA were: Age  <60  years; lost of consciousness shorter than
aneurysm, endovascular coiling demonstrated significantly 10 min; good general health condition; all patients in the
fewer severe cognitive deficits than surgical clipping. experimental group were HH Grade 1 or 2; all patients had
excellent neurological postoperative recovery; all patients
The goal of this research was to assess attention and executive were right‑handed, and all were operated by the single
functions in SAH patients after microsurgical clipping and neurosurgeon; all patients in the experimental group were
to compare their cognition with the cognition of the control operated on through the same surgical approach (pteryonal
group of patients treated by microdiscectomy due to lumbar craniotomy with transsylvian route.
disk herniation. In above-mentioned studies, researchers
Psychological assessment
used the control group of healthy patients. The variables that
In 1st time point, we used: Questionnaire to collect basic
partially caused the difference in cognitive functions between
information to the patient and the Trail Making Test (TMT)
clinical and healthy groups could have been an anxiety or
test of attention. In 2nd time point, we again use TMT, which
depression because of hospitalization. That is the reason why
gave us an opportunity to follow improvement with patients,
we use hospitalized patients as a control group. Cognitive
and we use other cognitive tests: The Sustained Attention
abilities of these two groups were tested in 2-time points:
to Response Task  (SART), Hayling Sentence Completion
10–12 days after the surgery and 46 days after the surgery.
Test  (HSCT), Attention/Concentration  (AC) test of attention,
Methods WAIS  (Comprehension) and WAIS  (Similarities) and Alcohol
Use Disorders Identification Test (AUDIT).
In this study, we controlled factors as age (there were no
patients beyond 60 years and there was no difference The TMT is a test of scanning and visuomotor tracking, divided
between control and experimental group), years of education, attention, and cognitive flexibility. It is given in two parts,
anesthesia, emotional and stress factors of being hospitalized, A and B. Slowed performance on TMT Part B relative to TMT
verbal intelligence, sex, premorbid loss of consciousness, Part  A signals impaired ability to execute and modify the
premorbid neurological or psychiatric illness, Hunt-Hess (HH) plan.[17] The SART is a continuous performance test developed
grade (only Grades 1 and 2), considering that all that factors by Robertson et al.[18] and involves the withholding of key
can be variables that can influence or moderate results on presses to rare  (one in nine) targets. The HSCT measures
cognitive function’s tests. As far as we know, there was no verbal response initiation and suppression.[19] Patients with
research conducted by the control group of hospitalized frontal lobe lesions need more time than control participants
subject that would give us an opportunity to exclude a factor in finding a word far from the semantic field that normally
of hospitalization on cognitive functions. completes the sentence.[20] The verbal part of WAIS[21] was used
to assess verbal intellectual function. AC test of attention is a
Subject characteristics continuous paper‑pan performance test where subject is asked
Two groups of patients were examined: 12 patients (7 male to cross letter C each time when he/she noticed that letter in
and 5 female), diagnosed with aneurysmal SAH treated with A4 paper among all other letters. The 10‑item AUDIT;[22] was
surgery and 12 patients after discus hernia surgery (5 male administered to assess alcohol use.
and 7 female).
Statistical analysis
All patients, in the time of testing, were middle-aged SPSS 17.0 (IBM company, Chicago, IL) software was used in the
(ME =45,92, SDE =8,81; MK =45, 50, SDK =12, 59; statistical treatment to the data. For tests used in both time
t = 0.094, df =22, P  =  0.926), with similar level of periods, we used mixed two (repeated measures for time:
education measured with years of school (ME =10,67, Spot 1 vs. spot 2) × 2 (SAH vs. DH) ANOVA (multiple analyses
SDE = 1,97; MK = 12,17, SDK = 1,80; t = −1.947, df = 22, of variance). For additional tests used during 2nd time period,

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Koso and Dizdarevic: Attention and executive function in SAH

we use t‑test. As an index of effect size, we report ²h that can control group, the experimental one shows statistically poorer
vary between 0 and 1. When ²h >0.15 effects are considered result on the sustained attention test measured by SART and
“large” in magnitude, and when ²h  0.06 effects are “medium.” AC. Time reaction, measured in seconds on SART test, shows
no difference between two groups. The experimental group
Results also achieved the significantly poorer results on HSCT, used
for the measurement of initiation, inhibition and evaluation
Visuomotor tracking and initiation (TMT A),
cognitive flexibility (TMT B, Hayling) and of the supervision attention system.
attention (SART, AC)
Factorial analysis of variance (2 × 2) for dependent variable Table 1: Descriptive statistical values for cognitive
cognitive attention and initiation [Table 1] we have attention and initiation
determined shoed statistically significant effects of factor Group First measurement Second measurement
Group (F = 16,103, P = 0.001) and time (F = 6,471, P = 0.019), Mean SD Mean SD
while the effect of interaction factor time × group is on the Experimental group 86.08 37.98 60.33 22.66
edge of statistical significance (F = 4,215, P = 0.052). Those Control group 40.00 17.62 37.25 16.41
that have undergone SAH surgery needed significantly more SD – Standard deviation

time for TMT A test than those with DH surgery. Furthermore,

both groups needed more time to solve TMT A in first than in Table 2: Descriptive statistical values for cognitive
the second measurement. T‑test for repeated measures has flexibility
confirmed that this change is statistically significant for the Group First measurement Second measurement
experimental group (t = 2,414 df = 11 P = 0.034), but not Mean SD Mean SD
for the control group (t = 0.803 df = 11 P = 0.439). Cognitive Experimental group 180.92 60.00 125.92 33.95
flexibility (TMT B) Control group 69.17 24.55 59.42 23.82
SD – Standard deviation
Factorial analysis of variance (2 × 2) for dependent variable
cognitive flexibility measured with TMT B [Table 2], Table 3: Descriptive statistical values, t‑values and effect
have determined statistically significant effects of factor size on tests SART, Hayling test, AC and WAIS memory
Group (F = 41,103; P < 0.01) and time (F = 19,566; P < 0.01),
Group Mean SD η²
as well as the effect of interaction factor factors (F = 4,215; SART f+ Experimental 10.33 6.29 t=1.675 (df=22; P=0.108)
P < 0.01). Those that have undergone SAH surgery needed Control 6.83 3.59
twice as much time to solve TMT B test than those with SART f− Experimental 30.25 32.81 t=2.264 (df=22; P=0.034) 0.179
DH surgery. Also furthermore, groups needed more time to Control 8.33 6.93
solve TMT B in first than in the second measurement. T‑test SART total Experimental 40.58 32.36 t=2.625 (df=22; P=0.015) 0.224
for repeated measures has confirmed that this change is Control 15.17 8.83
statistically significant for the experimental group (t = 3,957 SART rt Experimental 519.71 134.04 t=0.972 (df=22; P=0.341)
df = 11 P =  0.002). Values for the control group are also Control 472.96 98.87
on the edge of statistical significance (t = 2,124 df = 11 Hayling 1 Experimental 0.91 0.15 t=4.160 (df=22; P=0.0001) 0.427
P = 0.057). Control 0.71 0.056
Hayling 2 Experimental 2.98 1.88 t=3.602 (df=22; P=0.002) 0.359
Forty‑five days after SAH and DH surgeries patients were tested Control 1.01 0.197
with battery of tests for measurement of cognitive functions. Hayling index Experimental 3.24 1.82 t=3.273 (df=22; P=0.004) 0.338
We have used tests from the first measurement: TMT A and Control 1.42 0.28
TMT B, but also four additional tests: HSCT, SART, AC, sub tests AC L Experimental 39.42 2.78 t=−1.749 (df=22; P=0.094)
Comprehension and Similarities from WAIS. Results of those Control 40.83 0.39
AC R Experimental 40.00 1.86 t=−3.169 (df=22; P=0.004) 0.299
tests will be presented on following pages. Sustained attention,
Control 41.75 0.45
initiation, inhibition, vigilance and working memory Table 3
AC total Experimental 79.42 4.40 t=−2.465 (df=22; P=0.022) 0.205
shows means, standard deviations and t‑test for repeated
Control 82.58 0.67
measures for sustained attention, initiation, inhibition,
Control 7.83 1.85
vigilance and working memory [Table 3]. Descriptive statistical SART – Sustained attention to response task; SART f+ – Sustained attention to response
values, t‑values and effect size on tests SART, Hayling test, AC task false positive; SART f− – Sustained attention to response task false negative; SART
total – Sustained attention to response task total; SART rt – Sustained attention to
and WAIS memory. response task reaction time; Hayling 1 – Hayling sentence completion test part one,
Hayling 2 – Hayling sentence completion test part two; Hayling index – Hayling sentence
As Table 3 shows, there is statistically significant difference completion test relation between first and second part; AC L – AC attention test, number
of crossed letter on the left side; AC R – AC attention test, number of crossed letter on the
between the experimental and control groups on tests used right side; AC total – AC attention test, total number of crossed letters; WAIS – Wechsler
during the second measurement. When compared with the adult intelligence scale; AC – Attention/concentration; SD – Standard deviation

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Koso and Dizdarevic: Attention and executive function in SAH

Discussion between two measurements for the SAH group is much higher
and significant. All participants have been, in average, tested
According to current researches and theoretical presumptions, with an extended battery of tests for neuropsychological
we have assumed that patients, after clipping of ruptured assessment of cognitive functions 46 days after surgery and
intracranial aneurysm causing SAH, will experience certain 34 days after first testing. Apart from tests that have been used
cognitive dysfunction. We have also presumed that average during first measurement, such as attention assessment,
cognitive function test during the first measurement will be initiation and inhibition, cognitive flexibility, visuomotor
poorer than tests results achieved during the second activities, we have used additional test for assessment of
measurement, which implies that cognitive functions will sustained attention, verbal initiation, inhibition, vigilance,
recover in time. Results of cognitive function tests in patients working memory and verbal intellectual abilities. Table 3
after surgical treatment of aneurysm causing SAH have been indicates that there is statistically significant difference
compared with results of patients who have undergone lumbar between the experimental (SAH) and control groups with regard
disk microsurgery. Hospital time, stress, pre and postoperative to sustained attention where reaction time and sustained
anxiety and depression as well as postoperative recovery could attention were measured with SART test. Reaction time needed
represent variables that would influence results on the for completion of a task is slightly longer for the experimental
cognitive function test, which has not been controlled in group, but such difference is not significant. Total number of
researches before. In order to control the influence of such mistakes between control and experimental group is
variables, we choose the control group that has experienced significantly different. Another test that measures attention
general anesthesia and was operated on at the same and also represents a test of continued performance is AC test.
Neurosurgical Department. Data analysis indicates cognitive Table 3 indicates difference in the total number of crossed
dysfunction in SAH patients. According to Lezak[23] TMT is a test letters C. If we observe closely the number of crossed letters C
of scanning, visuomotor tracking, divided attention and on left and on the right side of the paper, we see that the
cognitive flexibility. It is a test of complex visual scanning where difference is not significant for the left side of the paper, but it
motor abilities, such as motor speed and agility, significantly is for the right one. Therefore, if we are to observe the number
influence test results. The same way as all other tests that of crossed letters C on the right side of the paper, we can notice
include motor speed and attention this one is very sensitive to that patients undergone aneurysm surgery make more mistakes
the brain damage.[23] Factorial analyses of variance have in this task and have significantly poorer sustained memory
confirmed that patients with aneurysm surgery needed and tracking. In our sample of patients with aneurysm surgery,
significantly more time to solve TMT An and TMT B test. Patients we have had seven patients with aneurysm on right and five
with SAH diagnosis that have undergone aneurysm surgery patients with aneurysm on the left side of the brain, which is
and have been tested on 12th and 46th day after the surgery had not significantly large sample for us to test significance of such
significantly poorer results on TMT test than patients tested difference between these two groups with regard to their
on 12th and 46th day after microdiscectomy. Effects of group, performance on cognitive tests. The HSCT is a measure of
time and interaction time × group are significant for TMT A response initiation and response suppression and is used for
and TMT B test. According to [Figures  1 and 2] functions assessing supervisory attentional system.[19] This function is
measured with TMT A and TMT B improved in time, but such controlled by the frontal lobe.[24] Our results indicate that
improvement is different for experimental and control group. patients after aneurysm surgery have extended reaction time
Difference between first and second measurement for the on first and second part of the test (initiation and inhibition)
control group is small and not significant, while the difference

Figure 2: Bigger and more significant changes in time for the

Figure 1: This graph shows significant changes in time for the experimental group (ΔMe = 55; ΔMk = 9, 75) compared with the
experimental group (ΔMe = 25, 75; ΔMk = 2, 75) than for the control one control group

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Koso and Dizdarevic: Attention and executive function in SAH

and ratio between these two measures is significantly higher before the surgery. Rehabilitation of SAH patients depends upon
for experimental  (SAH) than for the control group. Such our ability to recognize their problems and understand if and
difficulties result in slow reaction time for giving simple how cognitive deficits influence patients’ daily lives. If such
answers, inability to inhibit dominant response and supervision deficits are permanent and appear even after rehabilitation,
attention system disorder. Altogether, this result shows disorder the patient could be suggested to adopt new lifestyle and job.
of executive functions. Size of the effect is largest for HSCT that Patients with the memory disorder can be included in memory
measures initiation, inhibition and is presumably measure of rehabilitation programs. According to Wilson[29] memory
supervision attention system. Results that prove damaged rehabilitation, should not be focused upon the improvement
function of visuomotor memory, divided attention, cognitive on the test score for memory or any other neuropsychological
flexibility, sustained attention, verbal initiation, inhibition and functions. There are several basic steps in memory rehabilitation
vigilance for persons that have undergone aneurysm surgery process, including: Assessing memory and memory deficit,
is in accordance with results of many other authors whose providing relevant information to patients and family, agreeing
results also indicate a disorder of cognitive functions for on therapy goals and specific problems that will be treated,
aneurysm surgery patients.[9,10,11] Cognitive functions will choosing suitable external or internal strategies for a specific
recover in time, which can be concluded from this research and problem, teaching clients different strategies and evaluating
from researchers of other authors that have tested cognitive effects of the treatment.[29] Many authors emphasize the
functions in two or more time periods.[25] Due to the presence importance of support of community, family and work
of the control group that has also undergone general anesthesia colleagues.[9]
and operative stress, we can conclude that the reason for poorer
results on cognitive ability tests is SAH and aneurysm surgery. Obviously, neuropsychological assessment and treatment have
Other researchers that have included structural and functional to be an essential part of any recovery process for patients
brain scans could not explain or find any correlation of cognitive with SAH, including the initial phase (after aneurysm rupture
deficit. Even if there was a possibility to find areas in the brain and surgery). Early rehabilitation has to be available for all
affected with blood circulation disorder, there was no patients. During discharge rehabilitation, team must inform
correlation between location or brain hemisphere affected with patient and family on future treatment, continuous cognitive
aneurysm and cognitive dysfunction.[26] The SPECT study and behavioral therapy and social rehabilitation. It is also
conducted by Tooth et al.[27] identified a large common area of important to have additional assessment that will enable
subcortical hypoperfusion in the SAH patient undergone the rehabilitation team to re‑evaluate patient’s recovery,
surgery. Authors of this study suggest a possible link between social behavior and gather necessary information that will
reduced subcortical function and the extent and severity of help them plan all rehabilitation stages during SAH recovery.
cognitive deficits. Nozaki et  al.[28] determined cholinergic Improvement in daily practice with patients undergone
dysfunction in patients with cognitive impairment after SAH aneurysm surgery will not be possible without thorough
based on the pupillary response to tropicamide. There is also research on cognitive deficit causes.
an ongoing debate on mechanisms responsible for the recovery
of cognitive functions of stroke patients. Ponsford[29] presumes
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