European Journal of Neurology 2012, 19: 13611366

doi:10.1111/j.1468-1331.2012.03782.x

Early seizures in first-ever acute stroke patients in India:

incidence, predictive factors and impact on early outcome
R. P. Goswamia, P. S. Karmakarb and A. Ghoshc
a

Department of Medicine, Institute of Post Graduate Medical Education and Research, Kolkata; bDepartment of Medicine, North Bengal
Medical College and Hospital, Darjeeling; and cDepartments of Medicine and Rheumatology and Clinical Immunology, Institute of Post
Graduate Medical Education and Research, Kolkata, India

Keywords:

alcoholism, early
mortality, early seizures,
haemorrhagic stroke,
India, stroke
Received 29 January 2012
Accepted 4 May 2012

Background and purpose: Stroke-associated early seizures (ES) often complicate the
initial course of acute stroke. This study intended to estimate the rate of and the
predictive factors for ES and the impact of ES on the clinical outcome in patients
with rst-ever acute stroke.
Materials and methods: Consecutive patients with rst-ever acute stroke admitted
in the Department of Medicine from June 2010 to December 2011 were prospectively included. ES were dened as seizures occurring within 7 days from acute
stroke. Patients with history of epilepsy, transient ischaemic attack, subarachnoid
haemorrhage and cerebral venous thrombosis were excluded. Clinical outcomes
were measured under the subheadings of mortality and disability at discharge,
according to modied Rankin score.
Results: Of the 441 (56.92% male patients, median age 55 years, 49.43% had
haemorrhagic stroke) patients, 79 (17.91%, 95% condence interval (CI): 14.61
21.78%) suered from ES. At discharge, 37.64% were disabled, and 19.5% were
dead. In multivariate analysis, alcoholism, NIHSS at admission, haemorrhagic
stroke and cortical location were signicant predictors of ES. Thirty-day mortality
was predicted by NIHSS at admission [hazard ratio (HR): 1.14, 95% CI: 1.111.18,
P < 0.001], history of hypertension (HR: 3.79, 95% CI: 2.16.85, P < 0.001), history
of alcoholism (HR: 2.43, 95% CI: 1.493.95, P < 0.001) and early seizure (HR:
2.58, 95% CI: 1.544.34, P = 0.001).
Conclusions: Early seizures occurred in about 18% acute stroke patients. Alcoholism, haemorrhagic stroke, cortical and severe strokes predict development of ES. ES
are an independent important risk factor for early mortality.

Introduction
After ischaemic heart disease, stroke is the commonest
cause of mortality worldwide [1], causing nearly 5.7
million deaths in 2005 [2]. More than 80% of these
occurred in low- and middle-income countries [3].
Further, there may be 62 million survivors of stroke
worldwide, with up to a third living with severe disability [4].
Stroke, both ischaemic and haemorrhagic, has been
considered an important cause of epilepsy, especially
in the elderly [5,6].
Correspondence: R. P. Goswami, Abhyudoy Housing, Flat 18/14,
ECTP, Ph IV, Type B, EM Bypass, Kolkata, West Bengal
700107, India (tel.: +919433534335; fax: +913324331574;
e-mail: rudra.goswami@gmail.com).

2012 The Author(s)

European Journal of Neurology 2012 EFNS

Complications of acute stroke occurring during the

early days after the insult often determine the nal
outcome of events [7].
Stroke-associated early seizures (ES) are dened as
seizures occurring within 714 days after acute stroke
onset [811].
Seizures occurring after this are dened as late seizures. This distinction underlines dierences concerning pathophysiology, risk factors and impact on
disease course for early and late seizures [12].
Although a body of work has been done in the western world on this issue, there have been very few prospective studies regarding incidence of ES in stroke,
predictive factors for their development and impact
on outcome of stroke published from India [13].
This study intended to estimate the rate of and the
predictive factors for ES as well as the impact of ES

1361

1362

R. P. Goswami, P. S. Karmakar and A. Ghosh

on the clinical outcome in patients with rst-ever

acute stroke.

Materials and methods

Patients with rst-ever acute haemorrhagic or ischaemic stroke admitted in the Department of Medicine
from June 2010 to December 2011 were prospectively
and consecutively included in this study. Patients with
history of epilepsy or family history of epilepsy, and
patients with any past episodes of transient ischaemic
attack (TIA), subarachnoid haemorrhage (SAH) and
cerebral venous sinus thrombosis (CVST) were
excluded. Patients resenting for the rst time with
TIA, SAH or CVST were also excluded. The study
was approved by Institutional review board.
Stroke was dened according to the World Health
Organizations criteria, that is, sudden onset of signs
of focal or global disturbance of cerebral function
lasting more than 24 h with no apparent non-vascular
cause [14].
One or more CT scan images were obtained for all
patients and evaluated by the investigators, each unaware of the others interpretation. The study variables
were as follows: type of stroke: haemorrhagic versus
ischaemic versus haemorrhagic conversion of ischaemic stroke; site of the lesion: cortical versus subcortical; patients with both cortical and subcortical lesions
were considered cortical; prior lesions not related to
the current cerebrovascular episode were recognized
for the purpose of exclusion from the study. Patients
with no lesion in CT scan were put up for cerebral
magnetic resonance imaging with diusion weighted
images to look for ischaemic lesions.
Demographical variables (age and gender) and vascular risk factors such as history of hypertension, diabetes mellitus, hyperlipidaemia, history of ischaemic
heart disease and habitual factors (alcohol consumption > 50 gm/day, smoking) were collected from each
patient. Stroke severity was evaluated at admission
using the National Institute of Health Stroke Scale
(NIHSS) at admission. Clinical outcomes were measured under the subheadings of mortality and disability, according to modied Rankin score (mRS): 0, 1,
2: non-disabling stroke; 3, 4, 5: disabling stroke; 6:
death [15]. MRS was calculated both at discharge and
at 30th day of admission, and the latter value was utilized for survival analysis. ES were dened as seizure
occurring within 7 days from stroke onset, according
to the International League Against Epilepsy guidelines [16]. Seizures occurring at onset of stroke (onset
seizures) were excluded.
Early seizures predictors were assessed by univariate
analysis and multiple logistic regression analysis. Cate-

gorical baseline variables were analysed with chisquared test and continuous variables with Students
two-tailed t test. Statistical signicance was set at
P < 0.05. For multivariate analysis, risk factors were
entered in the model using a forward stepwise selection and setting at 0.05, the signicance level for
retention in the model that derived the maximum likelihood estimates of the odds ratio (OR) and the corresponding 95% condence interval for each variable.
For analysing the predictors of severe outcome in
univariate analysis, three groups were created (group
1: mRS = 0, 1, 2; group 2 = mRS 3, 4, 5; group 3 =
death). Continuous variables were analysed using ANOVA and post hoc analysis. Categorical variables were
analysed by the KruskalWallis test. In multivariate
survival analysis, Cox proportional hazard regression
was utilized. All analyses were performed with the
SPSS 16.0 (SPSS Inc., Chicago, IL, USA).

Results
A total of 441 [49.2% had haemorrhagic stroke
(n = 217), 48.8% had ischaemic stroke (n = 215), and
2% had haemorrhagic transformation of ischaemic
stroke (n = 9)] patients were enrolled in the study, of
which 79 (17.91%, 95% condence interval: 14.61
21.78%) patients suered from ES. Amongst the
patients, 56.92% were men. Median age of the population was 55 years (interquartile range 20 years).
Clinical and radiological predictors of ES were
analysed by univariate and multivariate statistics.
Details of univariate analyses are available at Table 1.
Of note, 23.5% [95% condence interval (CI): 18.33%
29.59%] of haemorrhagic stroke patients, 12.09%
(95% CI: 8.39%17.13%) of ischaemic stroke patients
and 22.22% (95% CI: 6.32%54.74%) of ischaemic
stroke patients with haemorrhagic transformation
developed ES (P = 0.008).
In multivariate logistic regression analysis, alcoholism [odds ratio (OR): 4.48, 95% condence interval
(CI): 2.099.63, P < 0.001], NIHSS at admission (OR:
1.06, 95% CI: 1.031.09, P = 0.001), haemorrhagic
stroke (OR: 2.58, 95% CI: 1.424.7, P = 0.002) and
cortical location (OR: 6.98, 95% CI: 3.8712.57,
P < 0.001) were signicant predictors of ES.
Amongst the 441 patients analysed, 189 patients
(42.86%) had mRS < 3, 166 patients (37.64%) had
mRS > 3, and 86 patients (19.5%) were dead. Regarding early outcome of stroke, ANOVA tables were created
between the three outcome groups (group 1: mRS < 3,
group 2: mRS > 3, group 3: death) for continuous variables (Table 2). Age, SBP and NIHSS at admission
values were signicantly dierent amongst the groups.
Post hoc analysis showed signicant age disparity

2012 The Author(s)

European Journal of Neurology 2012 EFNS European Journal of Neurology

Early seizures in acute stroke

Table 1 Demographical, clinical and radiological features of patients

with or without early seizure

Variable
Mean age in years
(SD)
Male (n)
Diabetes mellitus (n)
Hypertension (n)
Dyslipidaemia (n)
Ischaemic heart
disease (n)
Alcoholism (n)
Smoking (n)
Mean systolic blood
pressure in mmHg
(SD)
Mean diastolic blood
pressure in mmHg
(SD)
Haemorrhagic
stroke (n)
Ischaemic stroke (n)
Ischaemic stroke with
haemorrhagic
transformation (n)
Cortical lesion (n)
Mean NIHSS score
at admission (SD)
Mean duration of
hospital stay in
days (SD)

Without
convulsion
(n = 362)
54.38 (14.32)
56.91%
33.42%
61.33%
23.48%
22.65%

(206)
(121)
(222)
(85)
(82)

With
convulsion
(n = 79)
55.23 (14.66)
56.06%
43.04%
60.76%
18.99%
24.05%

(45)
(34)
(48)
(15)
(19)

P value
0.6
0.99
0.1
0.9
0.38
0.78

14.92% (54)
25.41% (92)
160.88 (29.54)

34.17% (27)
20.25% (16)
169.34 (36.09)

<0.001
0.3
0.02

101.15 (59.38)

107.01 (65.64)

0.43

45.85% (166)

64.56% (51)

0.002

52.2% (189)
1.9% (7)

32.9% (26)
2.2% (2)

0.0013
0.86

15.19% (55)
13.53 (8.18)

54.43% (43)
18 (9.85)

10.00 (5.49)

11.01 (7.85)

<0.001
<0.001
0.17

Tests of signicance: categorical variables chi-squared test, continuous variables Students two-tailed t test.

amongst groups 1 and 3 (P = 0.03). Mean SBP dierences amongst all the groups were signicant (group 1
versus group 2: P = 0.009, group 2 versus group 3:
P = 0.03, group 3 versus group 1: P < 0.001). Similarly,
NIHSS at admission was also signicantly dierent
amongst all the groups at signicance levels < 0.001.
Whilst analysing categorical variables, Kruskal
Wallis test was used amongst the three outcome
groups (Table 3). Presence of hypertension, alcoholism, ES and haemorrhagic stroke predicted early
disability or death.

1363

In Cox proportional hazard ratio model, 30 days

was predicted by NIHSS at admission [hazard ratio
(HR): 1.14, 95% CI: 1.111.18, P < 0.001], history of
hypertension (HR: 3.79, 95% CI: 2.16.85, P <
0.001), history of alcoholism (HR: 2.43, 95% CI: 1.49
3.95, P < 0.001) and early seizure (HR: 2.58, 95%
CI: 1.544.34, P = 0.001).

Discussion
In the present study, ES occurred in 17.91% of
patients with acute stroke. The principle conclusions
regarding the predictors of ES following stroke were
history of alcoholism, higher NIHSS at admission,
haemorrhagic stroke and cortical involvement. Interestingly, early mortality was strongly predicted by the
development of ES.
Symptomatic seizures have been reported to occur
in 233% of patients with acute stroke [1720]. The
reported wide range of percentages is probably
explained by the analysis of retrospective studies and
dierent window for dening ES (range 130 days)
[12]. Using a ceiling of 2 weeks to dene ES, incidence
has been reported to vary from 2.4% to 14% after
acute stroke in studies from western countries
[9,10,12]. Reported prevalence from Asian countries
varies as follows: 0.5% (Pakistan) [21], 2.5% (China)
[22], 9.41% (Thailand) [23] and 10.03% (India) [13].
No age or gender dierence was observed between
patients with or without ES. Although male sex and
age younger than 65 years have come up in certain
reports as predictive of ES [24,25], most of the earlier
reports do not assert this observation [9]. Consistent
with most reports, conventional vascular risk factors
(hypertension, diabetes mellitus, smoking, hyperlipidaemia or ischaemic heart disease) were not associated
with the development of ES [9,10].
However, alcohol consumption was signicantly
associated with ES. This eect was echoed earlier in
several reports by Leone et al. [26,27] who found that
alcohol consumption was a risk factor for acute symptomatic seizure after traumatic brain injury and
stroke.

Table 2 Demographical and clinical features of patients according to early functional outcome (ANOVA)

Variable

Rankin < 3
(n = 189)

Rankin > 3
(n = 166)

Death
(n = 86)

P value
(combined)

Age in years
Mean systolic blood pressure in mmHg
Mean diastolic blood pressure in mmHg
Mean NIHSS score at admission
Mean duration of hospital stay in days

53.07
154.96
94.56
8.56
8.61

54.51
164.52
106.78
16.7
13.92

57.79
174.63
110.16
22.88
6.42

0.04
<0.001
0.06
<0.001
<0.001

(14.20)
(25.58)
(14.76)
(5.76)
(4.47)

SD values are given in parentheses.

2012 The Author(s)

European Journal of Neurology 2012 EFNS European Journal of Neurology

(14.11)
(32.53)
(85.34)
(6.91)
(6.61)

(14.29)
(34.21)
(64.13)
(8.17)
(3.05)

1364

R. P. Goswami, P. S. Karmakar and A. Ghosh

Table 3 Demographical, clinical, biochemical and radiological features of patients according to early functional outcome (KruskalWallis test)

Male
Diabetes mellitus
Hypertension
Dyslipidaemia
Ischaemic heart disease
Alcoholism
Smoking
Percentage of patients with convulsions
Haemorrhagic stroke
Cortical lesions

Modied Rankin
score < 3 (n = 189)

Modied Rankin
score < 3 (n = 166)

Death (n = 86)

v2

P value

57.14% (108)
31.22% (59)
51.85% (98)
22.75% (43)
17.99% (34)
13.23% (25)
23.28% (44)
4.23%
44.44% (84)
16.93% (32)

57.22% (95)
40.36% (67)
60.84% (101)
26.51% (44)
28.92% (48)
17.47% (29)
27.11% (45)
22.89%
46.38% (77)
26.51% (44)

55.81%
33.72%
82.56%
15.12%
22.09%
31.39%
22.09%
38.37%
65.12%
25.58%

0.053
3.33
23.44
4.19
4.96
13.15
1.03
51.33
10.95
5.38

0.97
0.19
0.001
0.12
0.05
0.001
0.59
<0.0001
0.004
0.06

(48)
(29)
(71)
(13)
(19)
(27)
(19)
(56)
(22)

n, Values are given in parentheses.

Our result adds a positive data to the controversial

debate related to increased rate of ES in haemorrhagic
stroke. Although the evidence for increased rate of
seizure following haemorrhagic stroke is growing, signicant negative data were reported by Alberti et al.
[12] in 2008. Interestingly in 2009, Leoni et al. [27]
published a well-designed casecontrol study which
showed that haemorrhagic stroke is specically related
to ES rather than late-onset seizure following stroke.
They claimed that in acute state, presence of blood
acts as an irritant and generates higher rate of seizures
[8,9,27,28]. In 2011, another large study by Beghi
et al. reiterated that haemorrhagic stroke and cortical
involvement are independent predictors of ES in comparison with cerebral infarction with haemorrhagic
transformation. In their cohort (609 patients with
cerebral infarction with 32 cerebral infarction with
haemorrhagic transformation and 105 with intracerebral haemorrhage), 45 patients (6.3%) presented with
acute symptomatic seizures. In multivariate analysis,
primary intracerebral haemorrhage carried the highest
risk (OR 7.2) followed by cerebral infarction with
haemorrhagic transformation (OR 2.7) [29]. Whilst
16.2% of their patients with intracerebral haemorrhage and 16.2% of patients with haemorrhagic
infarction developed ES, 23.5% of our haemorrhagic
stroke patients and 22.22% of our ischaemic stroke
patients with haemorrhagic transformation developed
ES. The fact that we could not demonstrate a signicant relation of haemorrhagic infarction with ES is
probably related to very low sample size of haemorrhagic infarction patients (n = 9). De Herdt V et al.
working solely on haemorrhagic stroke patients demonstrated that the only factor associated with ES was
cortical involvement. However, ES, in their cohort,
did not inuence vital or functional outcome [30]. It is
also important to remember that haemorrhagic lacunar strokes are not usually associated with ES [31]. It
is interesting to note that clinical symptoms classically

associated with cardioembolic infarction, such as seizures at onset are not specic for cardioembolic stroke
[32]. Also, ES were not a predictive clinical factor of
in-hospital death in a recent study carried out in
patients with cardioembolic infarction [33].
The mechanism of seizure initiation by haemorrhage is not well established. Products of blood
metabolism, like haemosiderin, may cause focal cerebral irritation leading to seizures. During acute ischaemic injury, accumulation of intracellular calcium and
sodium may result in the depolarization of the transmembrane potential and lower the seizure threshold.
Local cerebral glucose utilization (LCGU) studies
demonstrated increased LCGU within hours around
an intracerebral haemorrhage [34]. There is also evidence regarding eect of intracerebral haemorrhage
on glutamate uptake or glutamate receptors. A recent
paper suggests that intracerebral haemorrhage, possibly via thrombin activation of protease-activated
receptors, activates Src gene that phosphorylates
NMDA receptors and other proteins that mediate
injury after ICH [34]. These associated with the eect
of haemosiderin, and the factors like dissection of
blood from subcortical to cortical planes and rebleeding may explain the increased rate of ES in intracerebral haemorrhage. The importance of cortical damage
in seizure initiation, despite earlier negative results
[17], has been emphasized in most current literatures
[9,10,19,28].
Our study showed that ES were signicantly more
frequent in stroke patients with cortical lesions than
in those patients without cortical involvement even
with multivariate analysis.
Lesion size [17] and stroke severity [34] have been
variably related to ES. The prospective Copenhagen
Stroke Study, which dealts with ischaemic stroke only,
found that stroke severity at admission (measured
with the Scandinavian Stroke Scale) was the only factor related to ES [35]. In 2006, Carrera et al. [36]

2012 The Author(s)

European Journal of Neurology 2012 EFNS European Journal of Neurology

Early seizures in acute stroke

using continuous electroencephalography in acute

stroke patients found that only initial stroke severity
assessed by NIHSS at admission was the only independent predictor of electrical epileptic activity. Negative reports regarding this variable have also been
reported, notably Labovitz et al. [9] in 2001 and Alberti et al. [12] in 2008. However, our data clearly
implicate initial stroke severity as an important predictive factor for the development of ES.
The inuence of post-stroke ES on functional outcome and mortality has been a debated issue. The
Copenhagen Stroke Study failed to show a statistically
signicant eect of ES on in-hospital mortality in their
ischaemic stroke cohort [35]. Alberti et al. [12] in 2008
also commented that ES do not seem to be associated
with an adverse outcome at hospital discharge after
acute stroke. On the other hand in 1997, Arboix et al.
studied 1099 consecutive stroke patients, of which
2.5% had developed ES. Mortality was signicantly
higher in the ES group (33.3% vs. 14%) [28]. The
same group reproduced similar worse prognostication
for ES patients in atherothrombotic stroke patients in
2003 [37]. However, the largest study in this regard, by
Burneo et al. employing 5027 patients, depicted a poor
prognosis of stroke patients with ES. Mean mRS at
discharge for their patients with and without seizures
was 4.41 and 3.15, respectively (P = 0.0001). Only 90
(65%) of patients with seizures at stroke presentation
remained alive upon discharge, compared with 4100
(84%) of those without seizures (P = 0.0001). Stroke
fatality at 30 days was higher amongst those with seizures (36.2% vs. 16.8%, P = 0.0001) [38].
Our results support the latter observation regarding
both disability and mortality following stroke. We
hypothesize that early epileptiform activity exerts its
deleterious eects by increasing the metabolic
demand, increased cerebral blood ow, glucose and
oxygen consumption resulting in increased lactate levels, causing a secondary brain damage.
The only study in this particular topic reported
from India dealt with both early and late post-stroke
seizures most of which were ES. The only statistically
signicant factor predicting ES was cortical involvement. They failed to document any mortality eect of
ES. However, the sample size in the ES group of that
study was only 20, thereby lowering the power of the
study [13].
Our study had several limitations. We only evaluated the earliest imaging (CT or MRI)-based diagnostic parameters, namely subtype of stroke and cortical
or subcortical location of lesion. However, our results
overlook certain imaging-based factor (size of the
lesion, cortical atrophy, oedema, mass eect, leukoaraiosis and haemorrhagic conversion), which might have

1365

inuence on both the development of ES and the functional outcome. So our results should be interpreted
with caution and needs to be conrmed in further
studies. We also could not employ EEG; some seizures
could have been missed or some paroxysmal non-epileptic events could have been called seizures. Also single-centre nature of our study might make our results
dicult to interpret in the general population.
Despite this, the relatively large sample size in our
study and the prospective study design are the major
advantages. Also being the rst study from India that
focuses on post-stroke ES and related morbidity and
mortality should raise viable questions for the future
works regarding the need for proper outlook, prevention and management of ES in this setting, thereby
inuencing public health policy in developing nations.
In conclusion, we have demonstrated relatively
higher frequency (17.91%) of post-stroke ES. In
Indian patients, conventional risk factors for ES apply
in similar fashion with the addition of alcoholism. In
this preliminary study on Indian patients, ES have
emerged as an independent important risk factor for
both post-stroke disability and 30-day mortality.

Acknowledgements
The authors sincerely acknowledge the encouragement
and support provided by the Director of Institute of
Post Graduate Medical Education, Kolkata, to continue the present work.

Disclosure of conflict of interest

The authors declare no nancial or other conict of
interests.

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2012 The Author(s)

European Journal of Neurology 2012 EFNS European Journal of Neurology

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