ORIGINAL ARTICLE

A new clinical score for the prognosis of status epilepticus in adults

!lez-Cuevasa, E. Santamarinaa, M. Toledoa, M. Quintanab, J. Salaa, M. Sueirasc, L. Guzmanc and
M. Gonza
J. Salas-Puiga

a
Epilepsy Unit, Neurology Department, Vall dHebron University Hospital, Universitat Autonoma de Barcelona, Barcelona; bNeurology
Department, Vall dHebron University Hospital, Universitat Autonoma de Barcelona, Barcelona; and cNeurophysiology Department, Vall
dHebron University Hospital, Universitat Autonoma de Barcelona, Barcelona, Spain

EUROPEAN JOURNAL OF NEUROLOGY

Keywords:
age, modified Rankin
Scale, prognosis, score,
status epilepticus
Received 25 January 2016
Accepted 8 June 2016
European Journal of
Neurology 2016, 0: 17
doi:10.1111/ene.13073
Background and purpose: The severity of status epilepticus (SE) has an impor-
tant impact in clinical outcomes. The Status Epilepticus Severity Score
(STESS) is a score for predicting mortality in SE at admission. The baseline
modified Rankin Scale (mRS) might be a prognostic factor for assessing the
short-tem outcomes of SE. Therefore, our aim was to evaluate the eectiveness
of mRS and whether its addition to the STESS improves the prediction of
mortality.
Methods: Consecutive patients with SE and aged >16 years were recruited
during 3 years. Receiver operating characteristic curves and a logistic regres-
sion model were developed to estimate the scores of the new score, designated
as modified STESS (mSTESS), and it was subsequently compared with the
STESS.
Results: In all, 136 patients were included. Mean age was 62.01 ! 17.62 (19
95) years, and 54% were male. The capacity of the STESS to predict mortality
was 74.3% (95% confidence interval 63.8%81.8%), whilst the capacity of the
mRS to predict mortality was 65.2% (95% confidence interval 54.2%76.2%).
The logistic regression model and receiver operating characteristic curves
enabled the classification of mRS as follows: 0, mRS = 0; 1, mRS = 13; and
2, mRS > 3. These values, when added to the other items of the STESS,
resulted in the mSTESS with scores between 0 and 8 points. The capacity of
the mSTESS to predict mortality was 80.1%. An mSTESS > 4 established an
overall accuracy of 81.8% for predicting mortality, which was considerably
higher than the overall accuracy of STESS 3 (59.6%).
Conclusions: The baseline mRS was associated with high mortality risk. It is
proposed to use mSTESS to improve the prediction of mortality risk in SE.

Identifying the clinical factors that predict the out-

Introduction
Status epilepticus (SE) is a serious medical emergency
with an incidence of 10"41 per 100 000 people [1,2]
and results in short-term mortality in 7%39% of
patients [35].
Correspondence: M. Gonz! alez-Cuevas, Epilepsy Unit, Neurology
Department, Vall dHebron University Hospital, Universitat
Autonoma de Barcelona, Passeig Vall dHebron 119-121, Barcelona
08035, Spain (tel./fax: +34 93 489 4257; e-mail:
montsegonzalezc@gmail.com).
This study is not industry sponsored.
come of patients with SE is important because these
indicators may also be useful for clinical decision-
making. Previous studies have focused on short-term
prognostic factors of SE and have demonstrated that
older age and acute symptomatic etiology are related
to a poorer outcome [3,5,6]. Results are less consistent
for other variables such as altered level of conscious-
ness [4], total duration of SE [7,8], time to treatment
or seizure duration before initiation of therapy [9]. A
recent study of serum concentrations of acute-phase
proteins measured early in SE revealed an indepen-
dent association between albumin serum levels and

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M. GONZALEZ-CUEVAS ET AL.
mortality [10]. Another recent study found that the
serum concentrations of procalcitonin levels measured
at SE onset are independently associated with unfa-
vorable outcome [11].
A simple clinical tool for predicting individual out-
comes before obtaining the results of diagnostic tests
was proposed by Rossetti et al. [12]. These researchers
developed a simple clinical score for the prognosis of
SE in adults (Status Epilepticus Severity Score, or
STESS) to use prior to initiating treatment. The score
consists of four variables that are available at presen-
tation: history of seizures, age, seizure type and con-
sciousness impairment. It was concluded that the
STESS could identify patients with a high probability
of survival after SE. Later, a prospective study by the
same group confirmed that the STESS is able to reli-
ably identify SE patients who are likely to survive and
proposed that, in these cases, an early aggressive treat-
ment could not be routinely justified, to reduce the
inherent risks that are related to an aggressive treat-
ment plan. However, the STESS has low predictive
value for bad outcomes and has a ceiling eect espe-
cially in patients older than 65 years without pre-exist-
ing epilepsy [12,13].
The modified Rankin Scale (mRS) is an objective,
reliable measure of disability or dependence in daily
activities of a patient. It is commonly used in the eval-
uation of patients with neurological emergencies, such
as stroke or SE, as a tool to measure their functional
state [14,15]. This state may on many occasions be
influenced by the presence of dierent comorbidities,
and some recent studies have suggested that coexisting
comorbidities might be associated with poor short-
term prognosis in SE [1618].
Therefore, it is hypothesized that the patients base-
line mRS may be a prognostic factor that determines
the short-term outcome of SE and that the inclusion
of the baseline functional condition of the patient (i.e.
the mRS) in the STESS can improve the prediction of
mortality.
Methods
A retrospective registry of all adult patients (16 years
of age and older) who experienced SE and were
admitted to our hospital between March 2011 and
March 2014 was analyzed. The local ethics committee
authorized the study without obtaining informed con-
sent from all patients.
Status epilepticus was defined as a condition result-
ing either from the failure of the mechanisms respon-
sible for seizure termination or from the initiation of
mechanisms which lead to abnormally prolonged sei-
zures after 5 min for tonic-clonic SE and 10 min focal
SE [19]. Patients with post-anoxic SE or incomplete
clinical data were excluded.
In addition to demographic characteristics, the type
of status (convulsive or non-convulsive), a previous
history of seizures, seizure semiology, level of con-
sciousness before treatment, SE etiology and baseline
mRS collected at arrival at the emergency department
were identified by interview of the patients family
and by the patients history.
Seizure semiology was classified according to the
worst manifestation prior to treatment (in descending
order of gravity: non-convulsive SE in coma, general-
ized convulsive, complex partial, myoclonic or absence
or simple partial). Level of consciousness prior to
treatment was categorized as alert, somnolent or con-
fused, stuporous and comatose. SE etiology was clas-
sified according to the last report of the International
League Against Epilepsy [19] as being acute
symptomatic, remote symptomatic, progressive symp-
tomatic or idiopathic/cryptogenic. Clinical outcome
was assessed at hospital discharge (dead or alive).
The mRS was scored as follows: 0, no symptoms; 1,
no significant disability despite symptoms (i.e. able to
carry out all usual duties and activities); 2, slight dis-
ability (i.e. unable to carry out all previous activities
but able to look after own aairs without assistance);
3, moderate disability (i.e. requiring some help but able
to walk without assistance); 4, moderately severe dis-
ability (i.e. unable to walk without assistance and
unable to attend to own bodily needs without assis-
tance); 5, severe disability (i.e. bedridden, incontinent
and requiring constant nursing care and attention) [17].
The STESS relies on the assessment of age, where
under 65 years of age is 0 points and 65 years of age
or older is 2 points; previous history of seizures is 0
and no previous seizures 1; severity of seizure type
(simple partial, complex partial, absence, myoclonic as
complicating idiopathic generalized epilepsy 0; gener-
alized convulsive 1; non-convulsive SE in coma 2);
and level of consciousness (alert or somnolent/con-
fused 0; stuporous or comatose 1). A score of 02 is
defined as favorable, which indicates a low risk of
death, and a score of 3 points or higher is defined as
unfavorable [12].
A prognosis was made according to the likelihood
of patient death before hospital discharge.
Statistical analysis
Statistical analysis was undertaken using SPSS Statis-
tics for Windows, version 17.0 (SPSS Inc, Chicago,
USA).
Prognosis was assessed according to the clinical out-
come (alive or dead) at discharge. To determine
2016 EAN

variables associated with mortality, statistical signifi-
cance was assessed by Pearsons chi-squared or Fish-
ers exact test for categorical variables and the
Students t or MannWhitney U test for numerical
variables. The cuto age with best sensitivity and speci-
ficity to predict mortality was determined through a
receiver operating characteristic (ROC) curve. ROC
curves were also obtained to assess the capacity of the
mRS, the STESS and the modified STESS (mSTESS)
to predict death. The predictive capacity was deter-
mined as the area under the ROC curve with a confi-
dence interval (CI) of 95%. A logistic regression model
was performed to assess the mRS and STESS as inde-
pendent predictors of death using the Hosmer and
Lemeshow statistic to assess the goodness of fit. The
score added to the STESS that was used to obtain the
final mSTESS scale was based upon the coecient val-
ues (b coecients) of the logistic regression after con-
sidering the results of the ROC curves for each cuto
point of mRS used to predict mortality. Sensitivities,
specificities, as well as positive and negative predictive
values (PPVs and NPVs) were calculated to evaluate
the prediction accuracy for the best cuto points of the
STESS and the mSTESS. The overall accuracy for the
cuto point of each scale was obtained using the pro-
portion of patients that were classified for the predic-
tion of mortality. An ROC curve was also performed
to establish cuto points of the mSTESS to classify
patients into dierent risks of mortality. MantelHaen-
szel v2 tests were used to test the homogeneity of the
odds ratio (OR) across strata. A P value <0.05 was con-
sidered to be statistically significant.
Results
Of the 162 patients who were registered as having SE,
136 were included and 26 were excluded due to insu-
cient clinical data (seven cases) or to hypoxic etiology
(19 cases).
The mean age was 62.01 ! 17.62 (1995) years,
and 54.4% of patients were males. Also, 60.2% of
patients had a de novo SE episode. The total mortality
was 22.1%. The most common etiologies of SE were
acute symptomatic (47.1%) and remote symptomatic
(32.4%), which was mainly secondary to vascular
(30.9%) and tumor (19.9%) lesions. Of the patients
who died, 14% were due to status itself (homeostatic
failure), 34% were from complications during hospi-
talization, mainly respiratory infections, and 52% died
due to the etiology causing the status (17% acute
stroke, 6% intracranial hemorrhage, 10% subarach-
noid hemorrhage, 10% meningitis, 3% encephalitis
and 6% due to traumatic brain injury leading to brain
edema).
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CLINICAL SCORE FOR STATUS EPILEPTICUS 3
The demographics and the most relevant clinical
variables of the cohort were classified by outcome and
are presented in Table 1. In the univariate analysis, it
was found that age, non-convulsive SE in coma,
marked consciousness impairment, etiology, the
STESS and mRS were associated with higher mortal-
ity.
The use of anesthetic treatment was also included
in the univariate analysis, and even though mortality
was higher in patients requiring anesthetics this dier-
ence was not statistically significant. Regarding age,
the best cuto point to predict mortality in our sam-
ple (ROC curve) was 70 years old (P = 0.003).
The results of the logistic regression analysis
showed that the STESS (OR 1.863, 95% CI 1.345
2.577; P < 0.001) and mRS (OR 1.459, 95% CI
1.0042.19; P = 0.047) were the only independent pre-
dictors of mortality. The data model had an excellent
goodness of fit (Hosmer and Lemeshow test,
P = 0.240) with a regression coecient of the STESS
[b 0.622, SE(b) 0.166] which is almost twice that of
the mRS [b 0.378, SE(b) 0.190].
Considering both the values of the coecients of
the logistic regression, where a higher weight in the
STESS was observed, and the results of the ROC
curve of mRS that was used to predict mortality
[where two good cutos were obtained, one very sen-
sitive >0 (sensitivity 96.4%, specificity 23.1%) and the
other very specific >3 (sensitivity 21.4%, specificity
94.4%)], it was possible to divide the mRS into three
groups, to which the following scores were assigned:
0, mRS = 0; 1, mRS = 13; and 2, mRS > 3. These
scores were added to the STESS of each patient. The
cuto point of age to 70 years old was also modified
following our ROC curve results regarding age.
Finally a new score that was variable between 0 and 8
points was obtained, the modified STESS (mSTESS;
Table 2). The STESS, mRS and mSTESS predictive
capacities are detailed in Fig. 1, where it is noted that
the mSTESS has a greater capacity to predict mortal-
ity (80.1%, 95% CI 70.6%89.6%) compared to
STESS (74.3%, 95% CI 63.8%81.8%).
The best cuto point to predict mortality in the
mSTESS was a score of 4. When the established cuto
of STESS 3 was compared, an improvement in the
capacity to predict death was found with a higher over-
all accuracy (81.8% vs. 59.6%), as shown in Table 3.
This new scale provides a better PPV than the
STESS, thereby allowing those patients with a higher
risk of mortality to be better identified. Furthermore,
in the ROC curve another cuto point was observed
that allowed the patients with a very low risk of death
(mSTESS < 02) to be qualified successfully, enabling
three types of patients to be dierentiated according
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M. GONZALEZ-CUEVAS ET AL.

Table 1 Variables of interest to predict risk of mortality

Total 136 (100%) Alive 106 (77.9%) Dead 30 (22.1%) P

Age (mean, SD) 62.01 (!17.6) 60.1 ! 17.2 68.5 ! 17.6 0.022
Male 74 (54.4%) 56 (52.8%) 18 (60%) 0.486
History of previous seizures 54 (39.7%) 46 (43.4%) 8 (26.7%) 0.098
Seizure type
SP or CP 80 (58.8%) 68 (64.1%) 12 (40%) 0.018
GC 42 (30.9%) 33 (31.1%) 9 (30%) 0.906
NCSEC 14 (10.3%) 5 (4.7%) 9 (30%) <0.001
Consciousness
Alert or somnolent/confused 92 (67.6%) 82 (77.3%) 10 (33.3%) <0.001
Stuporous or comatose 44 (32.4%) 24 (22.6%) 20 (66.6%)
mRS (median, IQR) 1 (12) 1 (12) 2 (13) 0.002
Etiologies
Acute symptomatic 64 (47.1%) 43 (40.6%) 21 (70%) 0.004
Remote symptomatic 44 (32.4%) 41 (38.7%) 3 (10%) 0.003
Progressive symptomatic 11 (8.1%) 10 (9.4%) 1 (3.3%) 0.455
Cryptogenic/idiopathic 17 (12.5%) 12 (11.3%) 5 (16.7%) 0.531
STESS (median, IQR) 3 (13) 2 (13) 3.5 (25) <0.001
Anesthetic treatment 41 (30.1%) 28 (26.4%) 13 (43.3%) 0.075

CP, complex partial; GC, generalized convulsive; IQR, interquartile range; mRS, modified Rankin Scale; NCSEC, non-convulsive status epilep-
ticus with coma; SP, simple partial; STESS, Status Epilepticus Severity Score.

Table 2 Modified STESS (mSTESS) 1.0

mSTESS
Score STESS
mRS
Consciousness
0.8 Reference line
Alert or somnolent/confused 0
Stuporous or comatose 1
Seizure type
SP or CP 0 0.6
Sensitivity

GC 1
NCSEC 2
Age (years)
<70 0 0.4
70 2
History of seizures
Area under
SE 95% CI
Yes 0 ROC curve
STESS (06) 0.743 0.054 0.6380.818
No 1 0.2 mRS (05) 0.652 0.056 0.5420.762
mRS mSTESS (08) 0.801 0.049 0.7060.896
0 0
13 1
4 2 0.0
Total 08 0.0 0.2 0.4 0.6 0.8 1.0
1 - specificity
CP, complex partial; GC, generalized convulsive; mRS, modified
Rankin Scale; mSTESS, modified Status Epilepticus Severity Score; Figure 1 Capacity of the new scale versus the STESS to predict
NCSEC, non-convulsive status epilepticus with coma; SP, simple mortality.
partial; STESS, Status Epilepticus Severity Score.

patients in the group with an mSTESS score of 34

to risk of death: mSTESS 02, low risk; 34, interme-
diate risk; >4, high risk (Fig. 2).
Whether the decision to start sedation was associ-
ated with mortality for dierent scores in the mSTESS
was also analyzed using a stratified analysis. Amongst
patients with an mSTESS score of 02 (low risk),
2.3% died following exposure to anesthetic drugs ver-
sus 9.1% of patients who were not exposed. Amongst
(intermediate risk), 21.2% of patients died in the
exposed to anesthetic drugs group versus 25% of
patients who were not. Amongst patients with an
mSTESS score >4 (high risk), 50% of patients died in
the unexposed group versus 70% of patients in the
exposed group. The dierences were not significant
amongst the dierent risk groups after obtaining an
estimate of a common OR score of 1.74 (95% CI

2016 EAN

Table 3 Comparison of test performances between STESS 3 and mSTESS > 4
Sensitivity (%) Specificity (%) PPV (%)
STESS 3 73.3 55.7 31.9
mSTESS > 4 50 90.4 58.3
CI, confidence interval; mSTESS, modified Status Epilepticus Severity Score; NPV, negative predictive value; OR, odds ratio; PPV, positive
predictive value; STESS, Status Epilepticus Severity Score.
Figure 2 Prediction of mortality based upon the mSTESS value
according to risk group.
0.664.57) with an elevated degree of homogeneity
between the groups (P = 0.264). Therefore, mortality
in our series did not depend on sedation, regardless of
the dierent mSTESS scores.
Discussion
From a therapeutic perspective, it is important to
have tools that enable an accurate prognosis of
patients with SE in an early stage. The STESS is a
useful tool in this regard and has already been vali-
dated in previous studies; however, this tool has a
ceiling eect, particularly in patients older than
65 years of age who do not have pre-existing epilepsy
[13,14,20].
The age of patients had been previously determined
by other studies to be an important risk factor for
mortality after SE [4,5,13,16]. Given that older
patients are less resistant to complications of SE and
its treatment, such as pneumonia, this could be one of
the reasons why these patients result in a higher inci-
dence of unfavorable outcomes.
To determine mortality in relation to age, Towne
et al. used a range of 30 years [7]. Rossetti et al. cate-
gorized into age younger than 65 years or 65 and
older [4,13]. In a recent study by Leitinger et al.
another score (the EMSE) was proposed for
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CLINICAL SCORE FOR STATUS EPILEPTICUS 5
Overall
NPV (%) accuracy (%) OR (CI 95%) P
88.1 59.6 3.452 (1.4108.451) 0.007
87.0 81.8 9.400 (3.50425.217) <0.001
predicting mortality in SE by classifying age into
seven groups by assigning specific scores for each dec-
ade of life (from age 21 to >80). Nevertheless, it was
observed that mortality rates might change over time
in relation to age and examples were cited of out-
comes in a population-based study that was con-
ducted between 1982 and 1986 and included patients
that were substantially worse than patients in a recent
study [20,21]. This was particularly true for patients
over 60 years of age. Therefore, the age score in the
EMSE and STESS should be adopted, especially
because there has been a significant improvement in
the survival rate of certain age groups. Conversely,
there were patients who, despite being young, may
have a higher risk of mortality in relation to their
medical history and basal condition. In our series the
best cuto point for predicting mortality was
70 years.
It has been demonstrated that comorbidities may
influence the prognosis of SE. Thus, it has been sug-
gested in previous studies that patients with a higher
number of comorbid conditions have a worse out-
come [16]. In another prospective study, the role of
pre-existing comorbidities on the outcome of patients
with SE (assessed with the Charlson Comorbidity
Index) was examined. It was found that this measure
was not independently related to outcome and
instead a model that included etiology, the STESS
and each variable of the Charlson Comorbidity
Index was proposed. This produced an excellent pre-
dictive model for mortality [17]. Data provided by
the EMSE suggest an important role for comorbidi-
ties [18].
Dierent comorbidities may impact on the func-
tional state of patients; therefore it is hypothesized
that the use of an easy and fast score such as the
mRS to evaluate the functional state at emergency
arrival could be useful for predicting the prognosis of
patients with SE. This score has been demonstrated to
be a useful tool in other neurological emergencies,
such as acute stroke [14].
In a very recent study performed to identify factors
influencing long-term outcome in refractory SE the
functional outcome was quantified using the mRS.
For every refractory SE episode two outcomes were
6 !
M. GONZALEZ-CUEVAS ET AL.
evaluated, one at discharge and one long-term out-
come, and compared to baseline mRS. In the results it
can be observed that patients who had a poor long-
term outcome had a slightly higher median in mRS
compared with patients with a good outcome [3 (14)
vs. 2 (04)], but this dierence was not statistically sig-
nificant (P = 0.233). However, this study focused only
on refractory SE [22].
In our series, it was observed that the baseline func-
tional condition that was also defined by the mRS
was independently associated with mortality in
patients with SE. By adding this variable to the
STESS (increasing the cuto point of age), a new
score was obtained: the modified STESS (4 mSTESS,
NPV 87.0%, PPV 58.3%, overall accuracy 81.8%).
This new score not only allowed the prediction of
mortality to be improved but also allowed patients
who had a very low risk of death (mSTESS 2) to be
classified.
With this new scale, it was observed that the ceiling
eect of the STESS decreases; e.g. a 70-year-old
patient without pre-existing epilepsy and a good base-
line situation (mRS = 0) would score 3 points on our
scale that would correspond to intermediate risk of
mortality and not as an unfavorable prognosis as in
the STESS. In addition the higher value of PPV in
our score allows us to better identify those patients
with a really higher risk of mortality.
On the other hand, a recent study performed for
intensive care unit patients with SE has shown that
the use of intravenous anesthetic drugs in SE was
associated with an increased relative risk of death
independent of possible confounders and without sig-
nificant changes in risk by dierent grades of SE
severity and dierent SE etiologies [23]. The analyzed
cohort of these studies was exclusively composed of
patients seen in intensive care units, thus potentially
limiting the generalizability. In our series, globally, a
higher mortality was observed in patients who
required the use of anesthetics as part of treatment;
however, this result was not statistically significant
(P = 0.075). Moreover the mortality in our series did
not depend on coma induction, regardless of the dif-
ferent STESS scores. This result is similar to that pre-
viously reported by Rossetti et al. [13]. It has to be
taken into account that our analyses had a retrospec-
tive design, and findings were not adjusted for all
known outcome predictors.
Following the methodology of Rossetti et al. [12,13]
etiology was not included in our new score because
the cause can only be determined after several exami-
nations that require a delay of up to several hours or
days, which can be crucial for therapeutic manage-
ment.
Other functional scales, such as the Barthel scale,
may be more reliable and less subjective in assessing
disability; however, these scales are longer and less
suitable for rapid patient assessment.
One limitation of this study is that it is a retrospec-
tive cohort series from a single center, and it has not
been validated. Another limitation is that mortality
was considered as the primary outcome and only clini-
cal factors were considered. Electroencephalogram pat-
terns and other variables that might influence the
results such as seizure duration before initiation of
therapy and total duration of SE were ignored because
the aim was to focus only on the factors that can be
evaluated very early in the first assessment of the
patient. Also, like many clinical studies, only mortality
on discharge was investigated and a longer period of
evaluation would be very interesting for future studies.
Conclusions
The STESS is a useful tool in predicting mortality in
patients with SE at admission; these predictions can
be improved by adding baseline disability, as assessed
by the mRS, and increasing the cuto point of age to
70 years. A new proposal, the modified STESS, can
be more accurate in the short-term prognosis of
patients with SE.
Acknowledgements
The authors thank the ER neurology and neurophysi-
ologist consultants of the Vall dHebron University
Hospital, Spain, for their help with data acquisition.
Furthermore, we want to thank Dr Andrea O. Ros-
setti for reviewing the manuscript and for advice.
Disclosure of conflicts of interest
The authors declare no financial or other conflicts of
interest.
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