AMJ Vol 9 No 1 March 2022-2.indd

Althea Medical Journal. 2022;9(1)

Comparison of Cognitive Function between Intracerebral
Haemorrhage Stroke Patients with and without Hypertensive Crisis

Mohammad Arianto Satrio Wicaksono,1 Cep Juli,2 Chandra Calista,2 Uni Gamayani,2
Aih Cahyani,2 Paulus Anam Ong2

1Faculty of Medicine Universitas Padjadjaran, Indonesia, 2Department of Neurology, Faculty of
Medicine Universitas Padjadjaran/Dr. Hasan Sadikin General Hospital, Bandung, Indonesia

Correspondence: Mohammad Arianto Satrio Wicaksono, Faculty of Medicine Universitas Padjadjaran, Jalan Raya
Bandung - Sumedang Km. 21 Jatinangor, Sumedang, Indonesia, E-mail: mohammad17009@mail.unpad.ac.id

Introduction

Stroke is a rapidly developing clinical sign
of focal or global disturbance of cerebral
function, lasting more than 24 hours or leading
to death, with no apparent cause other than
that of vascular origin.1 Stroke can be classified
into ischaemic and haemorrhage stroke.2
Intracerebral haemorrhage (ICH) stroke is a
subtype of haemorrhage stroke, characterized
by neurological dysfunction caused by a
focal collection of blood within the brain
parenchyma or ventricular system, which is
not caused by trauma.1 Although ICH accounts
for only 10–20% of all strokes, worldwide it

causes 50% of stroke-related mortality and
disability.3,4

Hypertension is one of the main risk
factors for intracerebral haemorrhage stroke.5
Uncontrolled hypertension can lead to
hypertensive crisis.6 A hypertensive crisis can
be defined as severe increase in systolic blood
pressure greater than or equal to 180 mmHg
and/or a diastolic blood pressure greater
than or equal to 120 mmHg.7 Intracerebral
haemorrhage can cause several negative
outcomes, including cognitive impairment.4
The mini-mental sate examination (MMSE) is
a widely used assessment tool to assess global
cognitive function. The MMSE has several

Althea Medical Journal. 2022;9(1):24–29

Abstract

Background: Intracerebral haemorrhage (ICH) stroke is characterized by neurological dysfunction,
caused by focal collection of blood within the brain parenchyma or ventricular system that is not caused
by trauma. Hypertension is one of the main risk factors for intracerebral haemorrhage. Hypertensive
crisis, which is a more severe type of uncontrolled hypertension may aggravate the cognitive outcomes.
The aim of this study was to compare cognitive function between intracerebral haemorrhage stroke
patients with and without hypertensive crisis.
Methods: This study was a retrospective comparative analytic study, combined with a case-control
study from August to November 2020. All medical records of patients with intracerebral haemorrhage,
who were admitted to Dr. Hasan Sadikin General Hospital Bandung in 2019, were collected. The total
score of mini-mental state examination (MMSE) which was recorded in the medical record was taken
and compared between groups using the Mann-Whitney test. The MMSE was conducted on the day of
discharge, and the minimum education level of the patients was elementary school.
Results: We found a total of 109 medical records with ICH, 67 of which were with hypertensive
crisis. The median MMSE score in the hypertensive crisis group was slightly higher than in the non-
hypertensive crisis group. Furthermore, there was no statistical difference in MMSE scores between
intracerebral haemorrhage patients with and without hypertensive crisis (p-value=0.439).
Conclusion: There is no difference in cognitive function between intracerebral haemorrhage patients
with and without hypertensive crisis. Further study is of great value to explore the relation between
intracerebral haemorrhage patients with and without hypertensive crisis.

Keywords: Cognitive function, hypertensive crisis, intracerebral haemorrhage

https://doi.org/10.15850/amj.v9n1.2368

Althea Medical Journal. 2022;9(1)

advantages, including brevity and good
validity, and has been translated and validated
into various languages.8

Intracerebral haemorrhage in the presence
of severe hypertension, such as a hypertensive
crisis tends to have a high risk of hematoma
expansion.9 Increased bleeding volume may
worsen cognitive function. This study aimed
to compare the cognitive function between

intracerebral haemorrhage stroke patients
with and without hypertensive crisis on
discharge day.

Methods

This study was a retrospective study with
a comparative analytic method of two
independent groups, using a case-control

Mohammad Arianto Satrio Wicaksono et al.: Comparison of Cognitive Function between Intracerebral Haemorrhage
Stroke Patients with and without Hypertensive Crisis

Table 1 Characteristics of Intracerebral Haemorrhage Patients with and without
Hypertensive Crisis

Characteristics

With Hypertensive
Crisis

(n=67)

Without Hypertensive
Crisis

(n=42) p-value

n % n %
Gender
Male
Female

31
36

46
54

19
23

45
55

0.916

Occupation
Unemployed
Student
Office worker
Entrepreneur
Farmer/Fisherman/Labourer
Others

41
0

15
4
4
3

61
0

22
6
6
5

22
1

15
2
1
1

52
2

36
5
2
2

0.452

ICH location
Right hemisphere
Left hemisphere
Frontal lobe
Parietal lobe
Temporal lobe
Occipital lobe
Brainstem
Cerebellum
Basal ganglia
Thalamus

30
36
1
9

13
0
4
3

19
23

45
54
1

13
19
0
6
5

28
34

24
17
2
6
7
3
1
2

13
12

57
41
5

14
17
7
2
5

31
29

0.209
0.178

X0.558
0.900
0.719

X0.055
X0.647
X1.000
0.772
0.531

Risk factor
Hypertension
Dyslipidemia
Diabetes mellitus
Ischemic heart disease
Atrial fibrillation

66
21
5
5
1

98
31
7
7
2

35
14
1
2
1

83
33
2
5
2

X0.005
0.829

X0.403
X0.705
X1.000

History of stroke
First time
Recurrent

52
15

77.6
22.4

31
11

73.8
26.2

0.650

Note: ICH= Intracerebral haemorrhage, all use chi-square test except x= Fisher’s exact test

Althea Medical Journal. 2022;9(1)

26 Althea Medical Journal March 2022

Table 2 Distribution of Age, Intracerebral Haemorrhage Volume, and Years of Education in
Patients with Intracerebral Haemorrhage Patients with and without Hypertensive
Crisis

Characteristic n With Hypertensive Crisis (n=67)

Without
Hypertensive Crisis

(n=42)
p-value

Age, median (IQR), years 109 55 (48–59) 54 (45–60.75) X0.462
ICH volume, median (IQR), mL 56 16.14 (5.95–23.75) 10.07 (4.30–22.6) X0.351
Years of education, median (IQR) 92 12 (6–12) 12 (9–12) X0.385

Note: ICH= Intracerebral haemorrhage, IQR= Interquartile range, X= Mann-whitney test

Table 3 Comparison of MMSE Score in Intracerebral Haemorrhage Patients with and without
Hypertensive Crisis

MMSE Score With Hypertensive Crisis (n=67)
Without

Hypertensive Crisis
(n=42)

p-value

MMSE score
Mean± SD
Median
Min-max

22.36±5.68
24

5–30

22.88±6.29
23.5
7–30

X0.439

Note: MMSE= Mini-mental state examination, ICH= Intracerebral haemorrhage, IQR= Interquartile range, X= Mann-
Whitney test

approach. Data were taken from medical
records of ICH patients. Data collection was
carried out from August 2020 to November
2020, after obtaining approval from the
Research Ethics Committee Universitas
Padjadjaran, with ethics number 027/UN6.
KEP/EC/2021.

We collected all medical records of ICH
patients with and without hypertensive crisis,
who were admitted to Dr. Hasan Sadikin
General Hospital Bandung from January 2019
to December 2019. Only subjects who had a
total score of Mini-Mental State Examination
(MMSE) conducted on discharge day, with a
minimum education level of elementary school
were recruited. The MMSE score was already
stated in the medical record. Medical records
with incomplete MMSE scores, decreased level
of consciousness on discharge day, deceased
patient, and aphasia were excluded from
this study. The included subjects were then
divided into two groups with and without
hypertensive crisis. Hypertensive crisis status
was determined by measuring blood pressure
recorded in the medical record and/or final
diagnosis by the doctor in charge.

The data were analyzed by IBM SPSS ver.25.
Data normality test using the Kolmogorov-
Smirnov method (n>50) was performed on

the group with hypertensive crisis, while
Shapiro-Wilk (n<50) was performed on the
group without hypertensive crisis. The Mann-
Whitney test was used to compare the total
MMSE scores between the two groups.

Results

From a total of 276 subjects with ICH during
study period, 109 (39.5%) were included in
this study. The data excluded were due to 52
subjects deceased (31.1%) which was 36.5%
subjects with hypertensive crisis and 63.5%
without hypertensive crisis. Other subjects
that were excluded were due to incomplete
data, consciousness, aphasia, and illiterate.

There were 67 subjects with hypertensive
crisis and 42 subjects without hypertensive
crisis with the female prevalence was higher
than male in both groups, 54% and 55%,
respectively (Table 1). The majority of
patients in both groups were unemployed
(61% and 52%). The main stroke location in
the group with hypertensive crisis was in the
left hemisphere (54%) and thalamus (34.%),
whereas the right hemisphere (57%) and
basal ganglia (31%) were the main locations in
non-hypertensive crisis group. In both groups,
hypertension had the highest prevalence

Althea Medical Journal. 2022;9(1)

of risk factors (98.5% and 83.3%) followed
by dyslipidemia (31% and 33%). Most of
the subjects in both groups had no previous
history of stroke (78% and 74%). There was
a statistically significant difference in the
incidence of hypertension (p<0.05) in both
groups.

The median age in the group with a
hypertensive crisis was higher than in the
group without hypertensive crisis (Table
2). The hypertensive crisis group had the
similar median education level as the non-
hypertensive crisis group. The median of
ICH volume in the hypertensive crisis group
was larger compared to the groups without
hypertensive crisis. There were no statistically
differences in age, ICH volume, and education
level between the two groups (p>0.05).

Furthermore, the median MMSE score in the
group with a hypertensive crisis was slightly
higher than the group without hypertensive
crisis (Table 3). For the normality test, we
performed the Kolmogorov-Smirnov method
on the group with hypertensive crisis, while
the Shapiro-Wilk on the group without the
hypertensive crisis. The distribution of data
showed abnormalities. Hypothesis testing was
conducted using the Mann-Whitney method
in both groups and there was no significant
difference between the two groups (p> 0.05).

Discussion

In this study, females were predominated in
both groups. This finding is consistent with
a previous descriptive cross sectional study,
which found that females are predominantly
prevalent.10 This condition could be due to
longer life span of women, as the incidence
of stroke increases with age.11 However, this
result might also due to the high prevalence
of male previously excluded in this study.
Interestingly, a meta-analysis study has
found that the incidence of intracerebral
haemorrhage in an Asian population is 15%
lower in female than in male, although the
difference was not statistically significance.3
According to a systematic review and meta-
analysis of 59 studies in 19 countries, the
incidence of intracerebral haemorrhage tends
to be higher in men.12 In this study, both groups
showed that the majority of patients had 12
years of education. A longitudinal study also
showed consistent findings in education levels,
which found that 63% of primary intracerebral
haemorrhage patients had 10 years or more
of education.4 However, these findings were
inconsistent with another study showing that

elementary school is the highest prevalence.10
Deep brain haemorrhage location tended

to occur in both groups, specifically in the
basal ganglia and thalamus. This could be due
to the high prevalence of hypertension in this
study.13 Intracerebral haemorrhage located in
deeper structures tend to occur in patient with
hypertension, with the most common site being
the basal ganglia (55%), followed by thalamus
(26%).9 In this study, left hemisphere lesions
tended to occur in the hypertensive crisis
group, while right hemisphere lesions tended
to occur in the non-hypertensive crisis group.
The importance of cognitive deficits is in the
left hemisphere and supratentorial lesions,
followed by the territory of anterior and
posterior cerebral arteries.14 Left hemisphere
lesions have a main role for most cognitive
domains, mainly in the language aspect, while
right hemisphere lesions are mainly associated
with visuospatial and executive functions.15

Hypertension is the most frequent
risk factor in patients with primary
intracerebral haemorrhage.4 Our study has
also demonstrated that hypertension is the
risk factor with the highest prevalence with
a significant difference between both groups.
This study has found that the majority of
stroke events in both groups are the first-time
stroke events. Previous study has also shown
that of spontaneous ICH patients, a previous
medical history of stroke or transient ischemic
stroke was found in only 15% of patients.13

In this study, the median age of hypertensive
crisis group was higher than non-hypertensive
crisis group. Possibly, it is caused by increased
arterial stiffness, which reduces the arterial
buffering capacity, leading to age-associated
changes in blood pressure.16 This study also
has found that the median of ICH volume in
hypertensive crisis group is higher than non-
hypertensive crisis group. It could be due to
the existing evidence supports that there is an
association between systolic blood pressure
and hematoma expansion.17 However, data on
education and ICH volumes were incomplete
and might interfere with the results.

The median MMSE score of hypertensive
crisis groups was slightly higher than the
non-hypertensive crisis group. This might be
caused by predominant female gender in the
non-hypertensive crisis group compared to
the hypertensive crisis group (55% and 54%).
Female is associated with vascular cognitive
impairment by related degenerative pathology
that would interact with vascular pathology.18
Recurrent stroke in the non-hypertensive crisis
group has a higher incidence compared to the

Mohammad Arianto Satrio Wicaksono et al.: Comparison of Cognitive Function between Intracerebral Haemorrhage
Stroke Patients with and without Hypertensive Crisis

Althea Medical Journal. 2022;9(1)

hypertensive crisis group (26% and 22%).
Patients with a history of stroke have a steeper
rate of cognitive decline. However, our study
has shown no significant difference in cognitive
function between the groups with and without
hypertensive crisis, contrary to other studies
showing that there is a relationship between
cognitive impairment and hypertension
severity.13,19 However, the study has some
limitations such as lack of evidence of a
temporal relationship between exposure and
outcome.19 In addition, there is no significant
difference in stroke location between the two
groups in this study. As the location of stroke,
especially the left hemisphere and cortical
lobe, it is an important factor for cognitive
function.

The limitation of this study could interfere
with the result of the study. The small sample
size is due to the large number of data excluded
due to the high mortality of patient and
incomplete data in this study. In addition, the
day of the MMSE test performed in each subject
is different, so that it might affect the results.
Furthermore, pre-stroke cognitive status is not
assessed in this study. Pre-existing cognitive
impairment is one of the strongest prognostic
factors for subsequent cognitive decline.13 The
duration of hypertension is also an important
determinant of cognitive impairment. There
is an adverse effect of increasing the duration
of hypertension on cognition.20 In this study,
the duration of hypertension is not assessed
which may interfere with the results.

In conclusion, there is no significant
difference in cognitive impairment between
the hypertensive group and the non-
hypertensive group. Further studies are
recommended to pay attention to factors such
as pre-stroke cognitive impairment, duration
of hypertension, and variability in blood
pressure. The MMSE score in this study has
shown a cognitive impairment in both groups.
Education about the risk of hypertensive crisis
is of great value to prevent stroke and further
cognitive impairment. Appropriate treatment
of ICH patients with and without hypertensive
crisis to prevent further cognitive impairment
is needed. In addition, further studies need
to be conducted on the relationship between
hypertensive crisis and cognitive function, to
assess whether there is a significant worsening
of cognitive function in the hypertensive crisis
condition.

References

1. Sacco RL, Kasner SE, Broderick JP, Caplan

LR, Connors JJ, Culebras A, et al. An updated
definition of stroke for the 21st century:
a statement for healthcare professionals
from the American Heart Association/
American Stroke Association. Stroke.
2013;44(7):2064–89.

2. Parmar P. Stroke: classification and
diagnosis. Pharmaceutical J [Online
Journal] 2018. [Cited 2021 July 15].
Available from: https://pharmaceutical-
j o u r n a l . c o m / a r t i c l e / l d / s t r o k e -
classification-and-diagnosis

3. Ikram MA, Wieberdink RG, Koudstaal
PJ. International epidemiology of
intracerebral hemorrhage. Curr
Atheroscler Rep. 2012;14(4):300–6.

4. Biffi A, Bailey D, Anderson CD, Ayres AM,
Gurol EM, Greenberg SM, et al. Risk factors
associated with early vs delayed dementia
after intracerebral hemorrhage. JAMA
Neurol. 2016;73(8):969–76.

5. An SJ, Kim TJ, Yoon BW. Epidemiology,
risk factors, and clinical features of
intracerebral hemorrhage: an update. J
Stroke. 2017;19(1):3–10.

6. Alshami A, Romero C, Avila A, Varon J.
Management of hypertensive crises in the
elderly. J Geriatr Cardiol. 2018;15(7):504–
12.

7. Suneja M, Sanders ML. Hypertensive
emergency. Med Clin North Am.
2017;101(3):465–78.

8. Myrberg K, Hydén LC, Samuelsson C. The
mini-mental state examination (MMSE)
from a language perspective: an analysis
of test interaction. Clin Linguist Phon.
2020;34(7):652–70.

9. Kumar S. Hypertension and hemorrhagic
stroke. Hypertens J. 2017;3(2):89–93.

10. Lofissa SP, Ong PA, Atik N. Demographic and
risk factors of intracerebral hemorrhage
stroke patients in Dr. Hasan Sadikin
General Hospital Bandung in 2007–2016.
Althea Med J. 2018;5(1):32–7.

11. Boehme AK, Esenwa C, Elkind MSV. Stroke
risk factors, genetics, and prevention. Circ
Res. 2017;120(3):472–95.

12. Poon MTC, Bell SM, Salman RA.
Epidemiology of intracerebral
haemorrhage. Front Neurol Neurosci.
2015;37:1–12.

13. Benedictus MR, Hochart A, Rossi C,
Boulouis G, Hénon H, Van Der Flier WM, et
al. Prognostic factors for cognitive decline
after intracerebral hemorrhage. Stroke.
2015;46(10):2773–8.

14. Danovska M, Peychinska D. Post-stroke
cognitive impairment–phenomenology

Althea Medical Journal March 2022

Althea Medical Journal. 2022;9(1)

and prognostic factors. J IMAB Annual
Proceeding Scientific Paper. 2012;18:290–7.

15. Sagnier S, Munsch F, Bigourdan A,
Debruxelles S, Poli M, Renou P, et al. The
influence of stroke location on cognitive
and mood impairment. A Voxel-Based
Lesion-Symptom Mapping Study. J Stroke
Cerebrovasc Dis. 2019;28(5):1236–42.

16. Rockwood MRH, Howlett SE. Blood
pressure in relation to age and frailty. Can
Geriatr J. 2011;14(1):2–7.

17. Qureshi AI. The importance of acute
hypertensive response in ICH. Stroke.
2013;44(6 Suppl 1):S67–9

18. Chen X, Duan L, Han Y, Tian L, Dai Q, Wang
S, et al. Predictors for vascular cognitive
impairment in stroke patients. BMC
Neurol. 2016;16:1–15.

19. Muela HCS, Costa-Hong VA, Yassuda MS,
Moraes NC, Memória CM, Machado MF,
et al. Hypertension severity is associated
with impaired cognitive performance. J
Am Heart Assoc. 2017;6(1):e1004579.

20. Power MC, Tchetgen Tchetgen EJ, Sparrow
D, Schwartz J, Weisskopf MG. Blood
pressure and cognition: factors that may
account for their inconsistent association.
Epidemiology. 2013;24(6):886–93.

Mohammad Arianto Satrio Wicaksono et al.: Comparison of Cognitive Function between Intracerebral Haemorrhage
Stroke Patients with and without Hypertensive Crisis