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Poststroke Seizures
Isaac E. Silverman, MD;
Lucas Restrepo, MD;
Gregory C. Mathews, MD, PhD
Arch Neurol. 2002;59:195-201.
ABSTRACT
Stroke is the most common cause of seizures in the elderly, and seizures
are among the most common neurologic sequelae of stroke. About 10% of all
stroke patients experience seizures, from stroke onset until several years
later. This review discusses current understanding of the epidemiology, pathogenesis,
classification, clinical manifestations, diagnostic studies, differential
diagnosis, and management issues of seizures associated with various cerebrovascular
lesions, with a focus on anticonvulsant use in the elderly.
EPIDEMIOLOGY
In population studies, stroke is the most commonly identified cause
of epilepsy in adult populations older than 35 years.1
In the elderly, stroke accounts for more than half of the newly diagnosed
cases of epilepsy in which a cause is determined, ahead of degenerative disorders,
brain tumors, and head trauma.1 From stroke
registry data, about 5% to 20% of all individuals who have a stroke will have
subsequent seizures,2-3 but epilepsy
(recurrent seizures) will develop in only a small subset of this group. Given
that, in each year, more than 730 000 people in this country have a stroke,
a conservative incidence of seizures after stroke is about 36 500 new
cases per year.
The largest and most rigorous methodological attempt to examine poststroke
seizures was the prospective multicenter report from the Seizures After Stroke
Study Group.2 The study enrolled 1897 patients
and found an overall incidence of seizures of 8.9%. Recurrent seizures consistent
with the development of epilepsy were rare, occurring in 2.5% of the patients,
but the mean follow-up was only 9 months.
Seizures may be a more common accompaniment of hemorrhagic rather than
ischemic stroke.
Bladin et al2 found the incidence of
seizures to be 10.6% among 265 patients with intracerebral hemorrhage vs 8.6%
among 1632 with ischemic stroke. In another prospective series,4
seizures occurred in 4.4% of 1000 patients, including 15.4% with lobar or
extensive intracerebral hemorrhage, 8.5% with subarachnoid hemorrhage, 6.5%
with cortical infarction, and 3.7% with hemispheric transient ischemic attacks.
A seizure was the presenting feature of intracranial hemorrhage in 30% of
1402 patients.5 Among 95 patients with aneurysmal
subarachnoid hemorrhage, the incidence rate of prehospital seizures was higher
(17.9%) than that occurring in the hospital (4.1%).6
CLASSIFICATION AND PATHOGENESIS
Seizures after stroke are classified as early or late onset, according
to their timing after brain ischemia, in a paradigm comparable to post-traumatic
epilepsy.2, 7 An arbitrary cut
point of 2 weeks after the presenting stroke has been recognized to distinguish
between early- and late-onset poststroke seizures.5, 8-9
Different characteristics and mechanisms of poststroke seizures, according
to their proximity to the onset of brain ischemia, have been proposed, but
no clear pathophysiological basis exists for the 2-week cut point.
Most early-onset seizures occur during the first 1 to 2 days after ischemia.
Almost half (43%) of all patients in the Stroke After Seizures Study experienced
a seizure within the first 24 hours after stroke.2
In a series restricted to early-onset seizures, 90% of the 30 patients had
ictal activity within the first 24 hours.10
Most seizures associated with hemorrhagic stroke also occur at onset or within
the first 24 hours.11
During acute ischemic injury, accumulation of intracellular calcium
and sodium may result in depolarization of the transmembrane potential and
other calcium-mediated effects. These local ionic shifts may lower the seizure
threshold.2, 12 Glutamate excitotoxicity
is a well-established mechanism of cell death in the experimental stroke model.
Antiglutamatergic drugs may also have a neuroprotective role in ischemic settings,
aside from the role of treating seizures.
The size of regional metabolic dysfunction may also be relevant in causing
early-onset seizures. In the setting of large regions of ischemic hypoxia,
high levels of excitotoxic neurotransmitters may be released extracellularly.
In studies of the postischemic brain in experimental animal models, neuronal
populations in the neocortex13 and hippocampus14 have altered membrane properties and increased excitability,
which presumably lower the threshold for seizure initiation. The ischemic
penumbra, a region of viable tissue adjacent to the infarcted core in ischemic
stroke, contains electrically irritable tissue that may be a focus for seizure
activity.
In addition to focal ischemia, global hypoperfusion can cause seizure
activity. Hypoxic-ischemic encephalopathy is one of the most common causes
of status epilepticus and carries a poor prognosis. Particularly vulnerable
to ischemic insult is the hippocampus, which is an especially epileptogenic
area.
In late-onset seizures, by contrast, persistent changes in neuronal
excitability occur. Replacement of healthy cell parenchyma by neuroglia and
immune cells may play a role in maintaining these changes. A gliotic scarring
has been implicated as the nidus for late-onset seizures, just as the meningocerebral
cicatrix may be responsible for late-onset post-traumatic epilepsy.2
An underlying permanent lesion appears to explain the higher frequency
of epilepsy in patients with late than early-onset seizures. As in post-traumatic
epilepsy,15 late occurrence of a first seizure
appears to carry a higher risk for epilepsy. In patients with ischemic stroke,
epilepsy developed in 35% of patients with early-onset seizures and in 90%
of patients with late-onset seizures.16 The
risk for epilepsy was comparable in patients with hemorrhagic stroke; epilepsy
developed in 29% of patients with early-onset seizures vs 93% with late-onset
seizures.5
The concept that cardiogenic emboli to the brain are more likely to
cause seizures acutely is controversial, with few supporting data. Among 1640
patients with cerebral ischemia,17 events attributed
to a cardiac source were most commonly associated with early-onset seizures
(16.6%), even compared with supratentorial hematomas (16.2%). However, the
definition of cardiogenic mechanism in this series was often based on nonspecific
criteria. Several authors have questioned the association of seizures with
cardioembolic events.3-4 Seizures
at onset were not a criterion in a data bank study of the cardiac causes of
stroke.18 Intuitively, there is no reason to
suspect that cardioembolic lesions would be more likely than emboli from large-vessel
sources to cause seizures, as cardiac and large-vessel emboli frequently involve
lesions to distal cortical branches. The mechanism by which cortical emboli
precipitate seizures is uncertain,12 but possibilities
include depolarization within an ischemic penumbra, rapid reperfusion after
the fragmentation and distal migration of the embolus,19
or a combination of both.
Cortical location is among the most reliable risk factors for poststroke
seizures.2 Poststroke seizures were more likely
to develop in patients with larger lesions involving multiple lobes of the
brain than in those with single lobar involvement.20
However, any stroke, including those with only subcortical involvement, may
occasionally be associated with seizures.20
Earlier studies, relying on less sensitive neuroimaging techniques, may not
have detected concomitant small cortical lesions that could cause ictal activity.
The mechanism by which deep hemispheric subcortical lesions, most commonly
due to small-vessel disease, cause seizures is not understood.2
Analogous to cortical involvement in ischemic stroke, a lobar site is
considered to be the most epileptogenic location in patients with intracerebral
hemorrhage. In a series of 123 patients,21
seizure incidence was highest with bleeding into lobar cortical structures
(54%), low with basal ganglionic hemorrhage (19%), and absent with thalamic
hemorrhage. Caudate involvement of the basal ganglia and temporal or parietal
involvement within the cortex predicted seizures.21
Hemorrhage due to cerebral venous thrombosis also commonly presents with seizures.
Parenchymal, often cortical, hemorrhage resulting from local venous congestion
is the likely cause of seizure activity.
The mechanism of seizure initiation by hemorrhage is not established.
Products of blood metabolism, such as hemosiderin, may cause a focal cerebral
irritation leading to seizures, analogous to the animal model of focal epilepsy
produced by iron deposition on the cerebral cortex.22
In subarachnoid hemorrhage, there is often extensive hemorrhage into the basal
cisterns, which directly contacts the frontal and temporal lobes. Patients
with subarachnoid hemorrhage also may have an intraparenchymal component to
the hemorrhage (Figure 1).
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Figure 1. Seizures after intracerebral and
subarachnoid hemorrhage. An 82-year-old woman presented with sudden-onset
headache, dysphasia, and right hemiparesis while receiving anticoagulation
therapy for chronic atrial fibrillation. Computed tomographic (CT) scan at
admission (A) demonstrates an acute left temporal lobe intraparenchymal hematoma,
with adjacent subdural and subarachnoid hemorrhage. The responsible lesion,
an aneurysm of the middle cerebral artery, was treated surgically. During
the postoperative period, she had episodes of right-sided facial twitching
associated with transient worsening of her aphasia. A postoperative CT scan
3 months later (B) showed a hypodense lesion of the midtemporal lobe in the
middle cranial fossa. Electroencephalographic (EEG) findings (C) demonstrated
focal spike waves, consistent with seizure activity, followed by focal slowing
and periodic lateralizing epileptiform discharge in the left hemisphere. Ref
indicates reference.
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The only clinical predictor for seizures after ischemic stroke is the
severity of the initial neurologic deficit. Greater initial stroke severity9 or stroke disability2
predicted seizures. By contrast, in the Oxfordshire Community Stroke Project,
only 3% of 225 patients who were independent 1 month after a stroke experienced
a seizure between 1 month and 5 years.23 Patients
presenting with greater neurologic impairment tend to have larger strokes
that involve wider cortical areas.
In retrospective studies, risk factors for seizures after subarachnoid
hemorrhage included middle cerebral artery aneurysms,24
intraparenchymal hematoma,25 cerebral infarction,26 a history of hypertension,27
and thickness of the cisternal clot.6 By contrast,
clinical predictors for seizures after intraparenchymal hemorrhage have been
lacking.2
Vascular lesions may cause seizures by other mechanisms. Seizures due
to arteriovenous malformations and aneurysms typically occur when these lesions
rupture, but these vascular lesions may cause seizures by directly irritating
adjacent brain parenchyma (Figure 2).
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Figure 2. Mass lesion causing focal seizures.
A 43-year-old woman presented to the emergency department after focal-onset
right-sided clonic movements, followed by loss of consciousness. Computed
tomographic scan with contrast demonstrated a giant aneurysm of the middle
cerebral artery with adjacent cerebral edema, contrast uptake into the aneurysm,
and an adjacent region in which a thrombus has formed. The patient underwent
successful craniotomy, with thrombectomy and aneurysm clipping.
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Finally, seizures associated with vascular lesions occur in the setting
of significant reperfusion after revascularization procedures, most commonly
carotid endarterectomy for chronic severe extracranial carotid stenosis. The
reperfusion syndrome, first described by Sundt and colleagues,28
includes transient focal seizure activity, atypical migrainous phenomena,
and intracerebral hemorrhage, although the clinical triad is often incomplete.
Onset of this rare syndrome ranges from several days to 3 weeks after revascularization29 and often is signaled by a new ipsilateral headache.30 Surgical correction of an arteriovenous malformation
may also cause intraoperative or postoperative hyperemia, with subsequent
seizures or hemorrhage.19, 31 By
contrast, arteriovenous malformations located in border-zone regions subject
to relatively low flow rates have a lower risk for hemorrhage.32
The reperfusion syndrome has been attributed to impaired cerebral autoregulation.19 In the setting of chronic hypoperfusion due to high-grade
carotid stenosis, the arterioles responsible for normal autoregulation in
the downstream cerebral hemisphere become chronically dilated. Subsequently,
when perfusion is improved by a revascularization procedure, the vessels are
incapable of vasoconstriction, and the brain parenchyma is subjected to a
massive augmentation of blood flow. The release of vasoactive neuropeptides
from perivascular sensory nerves may contribute to the development of the
reperfusion syndrome,19 to oxidants that develop
before revascularization,33 and to an inflammatory
response to the reestablishment of circulation.34
CLINICAL MANIFESTATIONS
Given that most poststroke seizures are caused by a focal lesion, poststroke
seizures are typically focal at onset. In a study of early-onset seizures
in 90 patients,17 simple partial seizures were
the most common type (61%), followed by secondarily generalized seizures (28%).
In other series,3, 10 early-onset
seizures were more likely to be partial, whereas late-onset seizures were
more likely to generalize secondarily. Most recurrent seizures are of the
same type as the presenting episode, and they tend to recur within 1 year
on average.
In a large series of patients with poststroke seizures, 9% had status
epilepticus.35 The only associated finding
was higher functional disability; status epilepticus was not associated with
a higher mortality rate, stroke type (ischemic or hemorrhagic), topography
(cortical involvement), lesion size, or electroencephalographic (EEG) patterns.
The phenomenological features of the reperfusion syndrome are similar
in that focal onset with occasional secondary generalization is the rule.
Seizure activity always occurs in the ipsilateral vascular territory of the
surgically treated internal carotid artery.28
Occasionally, status epilepticus ensues (Figure 3).
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Figure 3. Status epilepticus due to the
reperfusion syndrome. A 66-year-old woman underwent an otherwise uncomplicated
right carotid endarterectomy for asymptomatic extracranial carotid artery
disease 3 days earlier. She awoke with a headache, followed by left-arm clonic
movements. These progressed to generalized, tonic-clonic seizures, which were
not aborted by administration of lorazepam and phenytoin sodium therapy. The
continuous electroencephalographic (EEG) monitor showed periodic lateralized
epileptiform discharges occurring every 2 to 5 minutes, lasting a few seconds
(A). Subsequent T2- and diffusion-weighted magnetic resonance imaging studies
of the brain showed right-sided thalamic (B) and cortical lesions (C). Phenobarbital
sodium was then administered, which arrested seizure activity. Ref indicates
reference.
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DIAGNOSTIC STUDIES
Holmes36 found that patients with periodic
lateralizing epileptiform discharges and bilateral independent periodic lateralizing
epileptiform discharges on EEG after stroke were especially prone to the development
of seizures. Those patients with focal spikes also had a high risk of 78%.
Focal slowing, diffuse slowing, and normal findings on EEG, by contrast, were
associated with relatively low risks of 20%, 10%, and 5%, respectively. Other
work found that cortical involvement on results of neuroanatomical imaging
studies was more predictive of epilepsy than any single EEG finding.10
Focal slowing on EEG may simply reflect a wide region of ischemic or
infarcted tissue involving the cerebral cortex or subcortical territory. In
addition to neuroimaging, EEG may be helpful in the early evaluation of poorly
defined poststroke focal neurologic symptoms. In selected patients, focal
slowing may confirm the clinical impression of hemispheric ischemia and argue
against ongoing seizures as an explanation for an acute neurologic syndrome.
The absence of EEG abnormalities does not definitively exclude cerebral ischemia,
particularly in subcortical or subtentorial structures, or intermittent seizure
activity.
Uncommonly, seizures may mimic ischemia and infarction on neuroimaging
findings. Lansberg et al37 recently described
several acute magnetic resonance imaging findings in 3 patients with partial
status epilepticus. These studies showed cortical hyperintensity on diffusion-weighted
imaging and T2-weighted sequences and a corresponding area of low apparent
diffusion coefficient. However, these findings were readily differentiated
from typical ischemic stroke in their nonvascular distributions, increased
signal of the ipsilateral middle cerebral artery on magnetic resonance angiography,
and leptomeningeal enhancement on postcontrast magnetic resonance imaging.
Another study showed a hyperintensity on diffusion-weighted images in the
dorsolateral portion of the ipsilateral thalamus in 2 patients (Figure 3).38
DIFFERENTIAL DIAGNOSIS
The differential diagnosis of ischemia-induced seizures includes secondary
seizures due to other causes. Medications, drug therapy withdrawal (eg, benzodiazepines),
and metabolic disturbances (eg, glucose abnormalities) typically cause generalized
seizures, unless an underlying lesion is already present. Migraine-related
focal phenomena and transient ischemic attacks may produce focal slowing on
EEG findings. Among these entities, glucose abnormalities should not be overlooked.
MANAGEMENT
Choice of an anticonvulsant medication should be guided by the individual
characteristics of each patient, including concurrent medications and medical
comorbidities. To our knowledge, no controlled trials evaluating only poststroke
seizures have been conducted to assess specific agents. Perhaps a more important
issue is whether to initiate treatment at all, because only a few poststroke
seizures have been demonstrated to recur. In the absence of absolute predictors
of poststroke epilepsy, most physicians empirically treat patients for their
seizures when they occur in the setting of a recent stroke. Thus, Bladin et
al2 argue that a controlled trial including
patients with poststroke epilepsy would pose extensive logistical challenges
and would likely be unethical. Despite the relatively low incidence of poststroke
seizures, the absolute numbers are still high, arguing that an important problem
exists. Arboix et al39 concluded that the efficacy
of anticonvulsant prophylaxis should be assessed in prospective, randomized
trials conducted with high-risk patients.
Poststroke seizures are usually well controlled with a single anticonvulsant.
In 1 retrospective study, seizures in 88% of the 90 patients could be managed
with monotherapy.10 Given the typical focal
onset of poststroke seizures, first-line therapy options include carbamazepine
and phenytoin sodium. The latter has the advantage of parenteral administration,
which may be necessary given that swallowing or mental status likely will
be impaired. Fosphenytoin sodium is also a noteworthy option in stroke patients
because of lesser cardiotoxicity than phenytoin. Benzodiazepines, particularly
lorazepam, should be initially administered to the patient with ongoing seizures.
No data support the use of different agents to treat early vs late-onset seizures.
The newer antiepileptic drugs are being touted as first-line agents
for elderly patients because of their effectiveness and favorable side-effect
profiles. Approximately 10% of nursing home residents in the United States
receive antiepileptic drugs, most often for the treatment of seizure disorders.40 In a trial of newly diagnosed epilepsy in the elderly,
lamotrigine was recently demonstrated to be better tolerated and to maintain
patients free of seizures for longer intervals than carbamazepine.41 Although many of the newer anticonvulsants, eg, topiramate42 and levetiracetam,43
have been studied as adjunctive agents for refractory partial seizures, in
practice they are often used as monotherapy. Gabapentin has been shown to
be efficacious as monotherapy for partial epilepsy.44
For all antiepileptic drugs, the chief relevant dose-limiting adverse effect
is sedation, particularly in the elderly stroke patient.
Drug interactions are an important consideration, since most stroke
patients take multiple medications.40 The first-generation
antiepileptic agents undergo significant hepatic metabolism, and phenytoin
and valproic acid are highly protein bound. For example, the well-recognized
interaction of warfarin with phenytoin makes it difficult to maintain consistent
therapeutic ranges of both agents.
In its guidelines, the Stroke Council of the American Heart Association45-46 recommended uniform seizure prophylaxis
in the acute period after intracerebral and subarachnoid hemorrhage. For intracerebral
hemorrhage, seizure activity may result in further neuronal injury and contribute
to coma, although no clinical data support this recommendation.45
Patients with solely cerebellar or deep subcortical (eg, thalamic) lesions
are at very low risk for seizures and need not be treated. The guideline suggests
a dose of phenytoin sodium titrated by serologic levels (14-23 µg/mL),
with discontinuation of therapy after 1 month if no seizure activity occurs
during treatment.47 Patients with seizure activity
more than 2 weeks after presentation are at a higher risk for recurrence and
may require long-term seizure prophylaxis.48
Small retrospective studies suggest no benefit of prophylactic anticonvulsants
after aneurysmal subarachnoid hemorrhage.49
However, because of the relatively low risk associated with antiepileptic
therapy and the great concern about aneurysmal rebleeding, a clinical trial
addressing this issue may never occur. Long-term use of antiepileptic agents
is not recommended for patients with subarachnoid hemorrhage who do not have
seizures, but should be considered when at least 1 of several risk factors
is present.46
In the case of reperfusion syndrome, the critical preventive measure
is likely the aggressive control of systemic blood pressure.19
The role of antiepileptic therapy in this population of patients is unclear.
Seizures during the reperfusion syndrome sometimes respond to antiepileptic
drugs, according to anecdotal evidence,50 but
may be difficult to treat in the absence of heavy sedation. Some surgeons
empirically administer prophylaxis owing to the concern about seizures for
1 to 2 weeks after endarterectomy in patients with high-grade carotid stenosis.
Management of venous infarction often dictates administration of systemic
anticoagulation, and, recently, intrathrombus thrombolysis via endovascular
delivery has demonstrated success in selected patients.51
Authorities recommend instituting antiepileptic therapy only if seizures occur.52
PROGNOSIS
The impact of poststroke seizures on stroke outcomes is unclear, with
conflicting data from different case series. In 2 prospective studies, early-onset
seizures were not associated with higher mortality rates9
or worse neurologic deficits.4 Seizures were
associated with better outcomes on the Scandinavian Stroke Scale in another
series9; the authors postulated that seizures
were a manifestation of a larger ischemic penumbra that contributed to better
recovery. Conversely, in other work, patients who had early-onset seizures
within 48 hours of the presenting stroke or transient ischemic attack were
significantly more likely to die in the hospital (37.9%) vs those who did
not present with seizures (14.4%).39
For subarachnoid hemorrhage, seizures at onset predicted late-onset
seizures and poor outcomes, measured by disability 6 weeks later using the
Glasgow Outcome Scale.53 In an Icelandic population,
epilepsy was more frequent in patients with severe neurologic residua (48%)
compared with those without (20%).8
Seizures in the reperfusion syndrome are usually self-limited. Long-term
prognosis depends on the development of intracerebral hemorrhage. In a series
of 1500 carotid endarterectomies, hemorrhage developed in 11 patients, and
4 of these patients died.54
CONCLUSIONS
Poststroke seizures are a common and treatable phenomenon, whereas the
development of epilepsy is relatively rare. Cerebrovascular lesions associated
with the development of seizures include the following: intracerebral (parenchymal)
and subarachnoid hemorrhage and cerebral venous thrombosis, with or without
venous infarction; lesions involving the cerbral cortex; larger neurologic
deficits or disability at presentation; and revascularization procedures involving
the extracranial internal carotid artery. The treatment of poststroke seizures
is no different than the approach to treatment of partial-onset seizures due
to other cerebral lesions, and poststroke seizures usually respond well to
a single antiepileptic drug. Given their tolerability, the newer generations
of anticonvulsant agents hold promise in treating older patients. Given the
low incidence of poststroke epilepsy, there is no indication for seizure prophylaxis
in patients with acute ischemic stroke who have not had a well-documented
first event. The need for chronic anticonvulsant use should be evaluated periodically,
perhaps every 6 months. Despite the absence of clinical data documenting effectiveness,
most patients presenting with intracerebral or subarachnoid hemorrhage should
receive short-term antiepileptic prophylaxis.45-46
Future areas of research regarding poststroke seizures include assessing
their impact on initial lesion size and on delayed patient outcomes, determining
the appropriateness of chronic antiepileptic therapy after a single seizure,
and establishing risk factors for the reperfusion syndrome. Poststroke epilepsy
may also become an important basic model in research that aims to prevent
the transformation of injured cerebral tissue into an epileptic focus.
AUTHOR INFORMATION
Accepted for publication September 25, 2001.
Author contributions: Study concept and design (Drs Silverman, Restrepo, and Mathews); acquisition of
data (Dr Silverman); analysis and interpretation
of data (Dr Silverman); drafting of the manuscript (Drs Silverman and Restrepo); critical revision of the
manuscript for important intellectual content (Drs Silverman,
Restrepo, and Mathews); administrative, technical, and material support (Drs Silverman and Restrepo); study supervision (Dr Silverman).
We thank Richard H. Mattson, MD, for his critical review of the manuscript.
Corresponding author and reprints: Isaac E. Silverman, MD, The Stroke
Center at Hartford Hospital, 85 Seymour St, Suite 800, Hartford, CT 06106
(e-mail: isilver{at}harthosp.org).
From The Stroke Center at Hartford Hospital, Hartford, Conn (Dr Silverman);
the Cerebrovascular Program (Dr Restrepo) and The Johns Hopkins Epilepsy Center
(Dr Mathews), Department of Neurology, The Johns Hopkins University School
of Medicine, Baltimore, Md; and the Synaptic Physiology Unit, National Institute
of Neurological Disorders and Stroke, Bethesda, Md (Dr Mathews).
REFERENCES
| |
1. Hauser W, Annegers J, Kurland L. Incidence of epilepsy and unprovoked seizures in Rochester, Minnesota:
1935-1984. Epilepsia. 1993;34:453-468.
FULL TEXT
| PUBMED
2. Bladin C, Alexandrov A, Bellavance A, et al. Seizures after stroke: a prospective multicenter study. Arch Neurol. 2000;57:1617-1622.
FREE FULL TEXT
3. Davalos A, de Cendra E, Molins A, et al. Epileptic seizures at the onset of stroke. Cerebrovasc Dis. 1992;2:327-331.
4. Kilpatrick C, Davis S, Tress B, Rossiter S, Hopper J, Vandendriessen M. Epileptic seizures after stroke. Arch Neurol. 1990;47:157-169.
ABSTRACT
5. Sung C, Chu N. Epileptic seizures in intracerebral hemorrhage. J Neurol Neurosurg Psychiatry. 1989;52:1273-1276.
ABSTRACT
6. Rhoney D, Tipps L, Murray K, Basham M, Michael D, Coplin W. Anticonvulsant prophylaxis and timing of seizures after aneurysmal
subarachnoid hemorrhage. Neurology. 2000;55:258-265.
FREE FULL TEXT
7. Jennett B. Early traumatic epilepsy. Arch Neurol. 1974;30:394-398.
ISI
| PUBMED
8. Olafsson E, Gudnumdsson G, Hauser W. Risk of epilepsy in long-term survivors of surgery for aneurysmal subarachnoid
hemorrhage: a population-based study in Iceland. Epilepsia. 2000;41:1201-1205.
FULL TEXT
|
ISI
| PUBMED
9. Reith J, Jorgensen HS, Nakayama H, Raaschou HO, Olsen TS for the Copenhagen Stroke Study. Seizures in acute stroke. Stroke. 1997;28:1585-1589.
FREE FULL TEXT
10. Gupta S, Naheedy M, Elias D, Rubino F. Postinfarction seizures: a clinical study. Stroke. 1988;19:1477-1481.
FREE FULL TEXT
11. Berger A, Lipton R, Lesser M, Lantos G, Portenoy R. Early seizures following intracerebral hemorrhage: implications for
therapy. Neurology. 1988;38:1363-1365.
FREE FULL TEXT
12. Lambrakis CC, Lancman ME. The phenomenology of seizures and epilepsy after stroke. J Epilepsy. 1998;11:233-240.
13. Buchkremer-Ratzman |
