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Diffusion-Weighted Magnetic Resonance Imaging in Nonconvulsive Status Epilepticus
Kon Chu, MD;
Dong-Wha Kang, MD;
Joo-Yong Kim, MD;
Kee-Hyun Chang, MD;
Sang Kun Lee, MD
Arch Neurol. 2001;58:993-998.
ABSTRACT
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Background In human and experimental models, diffusion-weighted magnetic resonance
imaging (DWI) findings in status epilepticus (SE) have been reported to show
that apparent diffusion coefficients are reduced during the initial phase
and normalized or increased in the later phase of prolonged SE. This effect
is caused by cytotoxic edema induced by excitotoxicity. In humans, only focal
DWI abnormalities have been reported in partial SE.
Objectives To report and discuss the DWI findings suggesting diffuse neuronal injury
in a patient with nonconvulsive SE.
Design and Methods A 56-year-old man was admitted because of changing levels of consciousness
over 3 days. On admission he was comatose. He had nystagmoid eye movement,
forced eye blinking, and oroalimentary automatism. The results of a search
for possible infectious and metabolic etiologies were negative, and electroencephalographic
findings showed continuous, semirhythmic, bifrontal sharp waves of 2 Hz. Phenytoin
and midazolam hydrochloride were infused to alleviate the seizure activities.
He underwent DWI initially (3 days after the onset of seizure) and at the
5-month follow-up.
Setting The neurology department of a tertiary referral center.
Results During SE, DWI findings showed marked, diffuse gyriform cortical hyperintensity
throughout the brain. The apparent diffusion coefficient decreased in the
corresponding areas, especially in the occipital lobes. Findings from T2-weighted
magnetic resonance imaging showed the intense cortical hyperintensity with
gyral swelling and no involvement of brainstem, basal ganglia, thalamus, and
white matter. The follow-up DWI findings showed marked atrophy and hypointensity
in the corresponding regions. The apparent diffusion coefficient increased
in the corresponding regions.
Conclusions Diffusion-weighted imaging in our patient indicated that the magnetic
resonance imaging abnormalities of the affected cortex were due to cytotoxic
edema caused by neuronal excitotoxicity during prolonged SE. Diffusion-weighted
imaging can be used in the localization of seizure focus for predicting the
prognosis of the affected tissue and for researching the basic pathophysiology
of SE.
INTRODUCTION
STATUS EPILEPTICUS (SE) is one of the most common life-threatening neurologic
disorders. It is defined as "more than 30 minutes of (1) continuous seizure
activity or (2) 2 or more sequential seizures without full recovery of consciousness
between seizures."1 Data from animal studies
suggest that seizures lasting longer than 30 minutes may be associated with
increased neuronal injury.2 The pathophysiologic
characteristics of SE involve a complex interaction of excitatory and inhibitory
mechanisms, which both initiate and maintain generalized convulsive SE and
nonconvulsive SE.
Diffusion-weighted magnetic resonance imaging (DWI) is based on the
translational movement or diffusion of water,3, 4, 5
and has been known to identify early brain ischemic injury as a hyperintense
region.6 The apparent diffusion coefficient
(ADC), which is a measure of water diffusion and is independent of T1 and
T2 relaxation times, can be calculated. In the acute stage of cerebral ischemia,
the depletion of metabolic substrates leads to the failure of the sodium-potassium
ion adenosine triphosphatase pump and subsequently to cytotoxic edema. This
in turn hinders water diffusion.7 In animal
models, DWI abnormalities similar to ischemia have been reported in status
epilepticus.7, 8, 9, 10, 11, 12
An early decrease and late increase of the ADC have been observed. The mechanism
of the early decrease of the ADC has been proposed to be cytotoxic edema due
to excitotoxicity.
In humans, there have been a few reports of DWI abnormalities in partial
SE13, 14, 15, 16
in which DWI hyperintensities occurred in the epileptic foci. However, DWI
abnormalities suggesting diffuse neuronal injury in nonconvulsive SE have
not been reported in humans.
PATIENTS AND METHODS
CASE HISTORY
A 56-year-old man was admitted for altered consciousness. Three days
before admission, his family members found him unresponsive in the morning.
Gross convulsive movement was absent. They observed forced eye blinking, nystagmoid
movements in both eyes, and intermittent chewing movement. The patient was
afebrile and acyanotic. He had a history of pontine hemorrhage 4 years previously;
however, he had since enjoyed good health. He had no history of seizure or
hypoxic damage. He was admitted to another hospital on the day of onset.
In the emergency department at the initial hospital, the patient was
comatose and did not respond to painful stimuli. Vital signs, electrocardiographic
results, and laboratory findings, including those from arterial blood gas
analysis, were normal. He was not cyanotic and had no convulsive movement.
He had only eye movements and lip smacking. The results of brain magnetic
resonance imaging (MRI) performed at the hospital on the day of onset showed
diffuse high signal intensities and cortical swelling on the T2-weighted image
and no involvement of basal ganglia, thalamus, brainstem, or white matter.
The patient was diagnosed as having nonconvulsive SE, and diazepam was infused
intravenously but was not effective. The patient was transferred to our hospital
on the second day of onset.
On admission the altered consciousness, eye signs, and chewing movement
were persistent. Vital signs and laboratory findings were normal. The results
of a cerebrospinal fluid examination showed a normal cell count and chemistry
profile; IgG index was normal, and an oligoclonal band of cerebrospinal fluid
was negative. Cultures and smears were negative for bacteria, fungi, and mycobacteria.
Viral polymerase chain reaction and antibody analysis of cerebrospinal fluid
for herpes simplex virus, enterovirus, cytomegalovirus, and Epstein-Barr virus
showed negative results. The results of electroencephalography (EEG) performed
on the third day of onset showed continuous, semirhythmic, bifrontal sharp
waves of 2 Hz (Figure 1A). Continuous
EEG monitoring showed the sudden development of 8-Hz rhythmic waves on the
left temporal area (Figure 1B).
After a 42-second run of rhythmic activity, the neurologists (K. C. and S.
K. L.) observed a rhythmic chewing movement (oroalimentary automatism) (Figure 1C).
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Figure 1. A, Continuous, semirhythmic, sharp
2-Hz waves present in bilateral frontal leads. B and C, Sudden onset of rhythmic
8-Hz waves in the left temporal area. D, After a 42-second run of rhythmic
activity in the left temporal area, a rhythmic chewing artifact (oroalimentary
automatism) appears. These rhythmic activities and the subsequent oroalimentary
automatism were uncommonly observed during continuous electroencephalographic
monitoring. Avg indicates montage.
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Brain MRI (including T2-weighted, T1-weighted, fluid-attenuated inversion
recovery, and diffusion-weighted) and magnetic resonance (MR) angiography
were performed on the third day of onset. Phenytoin and lorazepam were infused
intravenously but did not correct the clinical status and EEG findings. A
continuous infusion of midazolam hydrochloride was tried, and when the dose
was increased to the extent of burst suppression, the eye signs disappeared.
Midazolam administration was continued for 2 days and then tapered. The results
of EEG performed on hospital day 6 showed a generalized, diffuse, and mixed
slowing of background activity. The administration of diphenylhydantoin and
valproic acid was continued, and he was discharged in a persistent vegetative
state on hospital day 60.
DATA ACQUISITION AND ANALYSIS
The patient underwent DWI with conventional MRI on a 1.5-T system (Signa
Horizon, Echospeed; General Electric Medical Systems, Milwaukee, Wis) equipped
with an echo planar imaging capability. Diffusion-weighted images were obtained
in the transverse plane using a single-shot echo planar spin echo pulse sequence
with 6500/107 milliseconds, 1 excitation, and 2 b values (0 and 1000 s/mm2). The diffusion gradient pulse duration was 31 milliseconds with a
gradient separation of 33 milliseconds and a gradient strength of 2.16 G/cm.
The diffusion gradients were applied simultaneously along 3 axes (x, y, z).
From the Stejskal-Tanner equation,2 the ADC
was calculated as the negative slope of the linear regression line best fitting
the points on the b value vs natural log plot, where the signal intensity
is from the image region of interest acquired at each b value. Maps of the
ADC were created using this calculation on a pixel-by-pixel basis.
RESULTS
During SE, DWI findings showed marked, diffuse gyriform cortical hyperintensities
throughout the brain. The signal intensities in the corresponding areas on
the ADC map were hypointense (Figure 2A-B). The ADC decrease ranged from 341 to 570 x 10-6 mm2/s
and was most severe in the occipital lobe. The spared cortex showed normal
ADCs (Figure 2B, arrow). The DWI
in the underlying white matter showed hypointense areas, and the corresponding
ADC increased. Absolute ADCs are summarized in Table 1. The T2-weighted and fluid-attenuated inversion recovery
images demonstrated diffuse cortical hyperintensities in the abnormal regions
on the DWI; elsewhere they showed normal white matter, basal ganglia, and
brainstem. The results from the MR angiography were normal. In the results
of the 5-month follow-up DWI (Figure 3A-B),
the cortical hyperintensities on the previous DWI were reversed, ie, hypointense
and accompanied by cortical atrophy and ventricular enlargement. Atrophy was
at its most severe in both occipital lobes, which had the lowest ADC during
SE. The ADC map showed diffuse hyperintensities. The low signal intensities
of the underlying white matter on the initial DWI were normalized.
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Figure 2. A and B, Results of the initial
diffusion-weighted image performed on the third day after onset shows diffuse,
gyriform cortical hyperintensities. Note the sparing of the basal ganglia,
thalamus, and brainstem. Regions of interest in which the apparent diffusion
coefficients (ADCs) were measured are marked as squares in the respective
lobes: 1, frontal lobe; 2, temporal lobe; 3, parietal lobe; 4, occipital lobe;
and 5, underlying white matter. The spared cortex showed normal ADCs (B, arrow).
C and D, The ADC map shows the low signal intensities in the corresponding
regions.
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ADCs at the Initial and Follow-up DWI*
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Figure 3. A-B, Follow-up diffusion-weighted
image performed at 5 months after onset shows diffuse low signal intensities
in the cortical regions and cortical atrophy. The atrophy is most severe in
the temporo-occipital lobes. C-D, Follow-up apparent diffusion coefficient
map shows diffuse high signal intensities in the corresponding cortical areas
(marked by squares).
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COMMENT
Our patient had nonconvulsive SE. The classification of the type of
seizure in our patient was rather obscured because of the time delay from
the onset to the diagnosis (3 days) and lack of convulsive movement. The definition
of nonconvulsive SE is still evolving, so it is difficult to determine the
complications associated with it, although classifications based on clinical
presentation and underlying pathophysiologic characteristics have been proposed.17, 18, 19, 20 According
to the classification, our patient can belong to the indeterminate group.
However, there was evidence of focal seizure onset in our patient. First,
the focal, rhythmic, 8-Hz waves preceded the rhythmic chewing movement. Second,
the ADCs differed in various lobes, with the lowest in the occipital lobe
and the highest in the frontal lobe.
During this study, we observed for the first time diffuse DWI abnormalities
of nonconvulsive SE in a human. The ADC during SE in our patient decreased
significantly, and there were some regional differences. We did not measure
the relative decrease of the ADC because of the bilaterally widespread cortical
involvement. The MRI findings of our patient were not possibly caused by cerebral
ischemia or hypoxic damage. The results of the MR angiography were normal.
The predilection site of the hypoxic-ischemic encephalopathy is basal ganglia
and thalamus, which was not involved in our case. Furthermore, such a "cortex
only" involvement is not possible in cerebral ischemia.
There have been previous reports of DWI abnormalities in experimental
SE models7, 8, 9, 10, 11, 12
and human epilepsia partialis continua.13, 14, 15
In rats, ADC decreases from 14% to 49% have been observed in kainate- or flurothyl-induced
SE.7, 8, 9, 10, 11, 12
Ebisu et al12 demonstrated that during the
time course of ADC decreases in kainate-induced SE models, decreased ADC was
observed at 12 hours, with little evidence of histologic or T2-weighted MRI
changes.12 Fujikawa21
reported that the longer SE was sustained, the more neuronal death occurred
in a pilocarpine-induced SE model. Righini et al10
observed that the initial decrease in ADC could be reversed, and the ADC later
increased. The area of hyperintensity on DWI was concordant with the histologic
distribution of neuronal pyknosis and neuropile vacuolation.11
The decrease in the ADC in SE is believed to be due to cytotoxic edema;
however, it cannot be a consequence of ischemia. In SE, cerebral blood flow
has been shown repeatedly to rise severalfold in most parts of the brain to
the highest level recorded during any condition.22
The ADC decline has been shown to correlate with a decrease in the extracellular
space volume fraction and an increase in extracellular tortuosity, both of
which are manifestations of massive cell swelling (ie, cytotoxic edema).23 The study of the N-methyl-D-aspartate–induced
excitotoxicity model demonstrated that the disorganization of the cytoplasmic
matrix can be crucial in raising intracellular obstacles.24
Swelling of cell organelles, disaggregation of polyribosomes, progressive
cytoplasmic and karyoplasmic condensation, proliferation of intracellular
membranes, and an increase in the number of cytoplasmic fibrillary structures
may contribute to an increased resistance to the mobility of intracellular
compounds.24 Wang et al9
reported an increase in sodium concentration in the pyriform cortex of rats
during SE. They proposed that this might have been due to an energy failure
of the sodium-potassium ion adenosine triphosphatase pump, which in turn could
lead to sodium ion and water influx. However, other studies that have found
increased oxygen pressure in the draining vessels of the epileptic region25 and no change in adenosine triphosphate levels26 do not support this hypothesis. Other proposed mechanisms
of cytotoxic edema in SE include excessive release of excitatory amino acids
(such as glutamate)27 and increased membrane
ion permeability.28
In our patient, the initial decline of the ADC was reversed during follow-up,
and cortical atrophy occurred in the corresponding areas. This is in accord
with several animal studies that have histologically demonstrated neuronal
cell death following SE21, 29 and
with 2 previously described human cases of radiologically confirmed brain
atrophy following SE.30 The possible cause
of increased ADC in follow-up DWI may be gliosis, extracellular volume expansion,
neuronal cell death, and partial volume effect.31, 32
Our patient had intractably prolonged nonconvulsive SE, resulting in neuronal
injury. The theoretical basis for neuronal injury resulting from nonconvulsive
SE may be identical to that from generalized convulsive SE; however, the underlying
pathophysiologic characteristics of the various subtypes of nonconvulsive
SE have not been investigated, so this remains speculative. There is evidence
of neuronal injury in complex partial SE and nonconvulsive SE associated with
severe brain injury.20, 33, 34, 35
Some areas in the frontoparietal lobes of our patient were spared at
the time of the initial and follow-up DWI. These findings suggest that more
selective involvement can occur, even in diffuse EEG change. The ADCs of the
occipital lobes were much lower in the initial study, and the cortical atrophy
was the most profound finding in the posterior temporal and occipital lobes
in the follow-up. Persistent eye blinking and nystagmoid eye movements might
be explained by the greater involvement of the occipital lobes. The reason
why the occipital predilection occurred is not understood. We would like to
suggest some explanations: First, the patient's initial seizure onset might
be in the occipital lobe and precede the secondary generalization. Second,
occipital involvement might have been due to spreading from elsewhere, such
as the temporal lobe. Ebisu et al12 reported
that their observations by MR spectroscopy and DWI, which showed little histologic
change, suggested that these modalities may detect epileptic foci. Signal
changes were present in regions known to exhibit electrographic seizure activity
in this model.36, 37 In contrast,
signal abnormalities were not present in regions that are not susceptible
to kainate. Zhong et al38 observed that the
ADC of brain water rapidly decreases in portions of the brain after cortical
electric shocks and that the magnitude of the drop in seizure-related ADC
correlates with the duration of brain activation. In their experiment, 10
seconds of bifrontal electroshock resulted in a 14% drop. Stimulation for
shorter periods caused smaller changes. Only portions of the parietal and
temporal lobes showed changes, not the whole brain. This suggests that the
volume of cortex with an altered ADC might define regions of chronically discharging
tissue in an epileptic brain.39, 40
Hence, all this evidence suggests that DWI may play a crucial role in clarifying
the epileptic focus and predicting the clinical or histologic prognosis, even
in cases with diffuse EEG changes.
Wieshmann et al13 observed that the ADC
of underlying white matter increased 27%; however, Lansberg et al14 reported normal ADCs in white matter. The ADCs of
the white matter in our patient increased (1338 ± 64 x 10-6mm2/s). Our findings are concordant with those of Wieshmann
et al13 and with experimental studies that
showed vasogenic edema in the underlying white matter.41, 42
Wieshmann et al suggested that a possible mechanism involved water shift,
which is caused by a breakdown of the blood-brain barrier.41, 42
During SE, the extracellular space expands in areas remote from the neuronal
activity,40 and this may explain the increase
in the ADC in white matter.
Diffusion-weighted imaging in our patient indicated that the MRI abnormalities
of the affected cortex were due to cytotoxic edema caused by neuronal excitotoxicity
during prolonged SE. Our findings suggest that DWI can be used to locate the
seizure focus and arrive at the tissue prognosis as well as research the basic
pathophysiologic characteristics of SE.
AUTHOR INFORMATION
Accepted for publication on December 11, 2000.
From the Departments of Neurology (Drs Chu, Kang, and Lee) and Diagnostic
Radiology (Dr Chang), Clinical Research Institute (Dr Chu), Seoul National
University Hospital, and the Neuroscience Research Institute, Seoul National
University Medical Research Institute (SNUMRC) (Dr Chu), Seoul, South Korea;
and the Department of Neurology, College of Medicine, Kangwon National University,
Choon-chon, South Korea (Dr Kim).
Reprints: Sang Kun Lee, MD, Department of Neurology, Seoul National
University Hospital, Clinical Research Institute, Neuroscience Research Institute,
Seoul National University Medical Research Institute, 28, Yongon-dong, Chongno-gu,
Seoul 110-744, South Korea (e-mail: 630106{at}medicampus.co.kr).
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