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Diffusion-Weighted Imaging Abnormalities in Wernicke Encephalopathy
Reversible Cytotoxic Edema?
Kon Chu, MD;
Dong-Wha Kang, MD, PhD;
Han-Joon Kim, MD;
Yong-Seok Lee, MD, PhD;
Seong-Ho Park, MD, PhD
Arch Neurol. 2002;59:123-127.
ABSTRACT
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Background Wernicke encephalopathy (WE) is a metabolic disorder of the central
nervous system resulting from vitamin B1 deficiency. The exact
mechanisms underlying the pathogenesis of the lesions in WE are not completely
understood. Vitamin B1 deficiency is associated with intracellular
and extracellular edema by glutamateN-methyl-D-aspartate receptor–mediated
excitotoxicity. Conventional magnetic resonance imaging (MRI) cannot differentiate
the types of edema. Diffusion-weighted imaging (DWI) has been reported to
detect early ischemic damage (cytotoxic edema) as bright areas of high signal
intensity (SI) and vasogenic edema as areas of heterogeneous SI.
Objectives To describe the DWI findings and to characterize the types of edema
in WE using DWI.
Setting Tertiary referral center.
Design and Methods Two patients with WE underwent DWI and conventional MRI with gadolinium
enhancement. Wernicke encephalopathy was diagnosed with salient conventional
MRI findings (high SIs in the paramedian thalamus, periaqueductal gray matter,
and mamillary bodies) and typical clinical history and symptoms. Apparent
diffusion coefficient (ADC) values were measured in abnormal lesions by visual
inspection of DWIs and T2-weighted echo planar images.
Results T2-weighted and fluid-attenuated inversion recovery MRIs showed high
SIs in the bilateral paramedian thalamus, mamillary bodies, and periaqueductal
gray matter. The DWIs showed bright high SI in the corresponding lesions,
and ADC values were decreased (patient 1: 512-545 x 10-6mm2/s; patient 2: 576-612 x 10-6mm2/s). The ADC decrease and the DWI high SI were normalized in 2 weeks
with administration of thiamine hydrochloride.
Conclusions Abnormalities on DWI and ADC decrease became normalized with adequate
therapy. The MRI abnormalities in WE might be owing to the "reversible cytotoxic
edema" caused by vitamin B1 deficiency.
INTRODUCTION
DIFFUSION-weighted imaging (DWI), first developed by Le Bihan et al,1 can detect changes in water diffusion associated with
cellular dysfunction and can also be used to detect ischemic lesions of the
brain within the first few hours.2 The application
of DWI in diagnosing arterial stroke is well established and has been demonstrated
by numerous experimental and clinical studies3-9
as an early decrease and late increase, or pseudonormalization, of the apparent
diffusion coefficient (ADC). It has been well documented that cytotoxic edema
related to acute infarction is characterized by markedly decreased diffusion
and that the increased interstitial water in vasogenic edema is seen as increased
diffusion. Conventional magnetic resonance imaging (MRI) cannot differentiate
between vasogenic and cytotoxic edema.
Wernicke encephalopathy (WE) is a disorder of the central nervous system
with characteristic neuropathologic changes. The illness results from a deficiency
of vitamin B1 (thiamine hydrochloride). The typical pathologic
findings include atrophy of the mamillary bodies; dilatation of the third
ventricle and aqueduct; and, microscopically, endothelial swelling in the
capillaries, microglial activation, petechial hemorrhage, and necrosis of
the periventricular gray matter of the hypothalamus, thalamus, periaqueductal
region of the midbrain, floor of the fourth ventricle, and cerebellum.10-11 The changes are often reversible
with adequate administration of thiamine.
There have been numerous articles12-17
concerning the MRI findings of WE. These findings are summarized as high signal
intensities (SIs) on T2-weighted and fluid-attenuated inversion recovery (FLAIR)
MRIs in the involved areas, such as the thalamus, hypothalamus, periaqueductal
gray matter and cerebellum, and gadolinium-enhancing lesions, indicating blood-brain
barrier breakdown. However, DWI findings have not yet been reported in WE,
to our knowledge. We report DWI findings and the analysis of ADC maps for
researching the pathogenesis of the edema in WE.
PATIENTS AND METHODS
DATA ACQUISITION AND ANALYSIS
Patients were examined using a 1.5-T MRI unit (Signa Horizon, Echospeed;
General Electric Medical Systems, Milwaukee, Wis) with echoplanar imaging
capability. Fast spin-echo, T2-weighted images (repetition time/echo time,
4200/112 ms; field of view, 21 x 21 cm; matrix, 256 x 192; and
slice thickness, 5 mm with a 1.5-mm gap) were obtained. Diffusion-weighted
imaging was obtained in the transverse plane using single-shot echoplanar
imaging (repetition time/echo time, 6500/125 ms; field of view, 24 x
24 cm; matrix, 128 x 128; slice thickness, 5 mm with a 2.5-mm gap; and
2 b values, 0 and 1000 s/mm2). The diffusion
gradients were applied along 3 axes (x, y, and z) simultaneously. The ADC
was calculated based on the Stejskal-Tanner equation18
as the negative slope of the linear regression line best fitting the points
for b vs ln (SI), where
SI is the signal intensity from the region of interest within the images acquired
at each b value. Performing this calculation on a
pixel-by-pixel basis created ADC maps. The respective ADC values are described.
Normal ADC values of the parenchyma and white matter range from 0.78 to 0.91
x 10-3mm2/s (K.C. and D.-W.K., unpublished
data, 2000). Regions of interest were carefully drawn in the abnormal areas
on calculated average ADC maps and in normal-appearing areas with variable
sizes. Small circular regions of interest of 9 to 25 mm2 were centered
on areas with abnormal signal on the DWIs or T2-weighted images to calculate
mean ADC values. Regions of interest were selected using T2-weighted echo-planar
images of the same acquisition as the DWIs (ie, images generated from the
diffusion sequence with diffusion sensitivity b =
0) to avoid errors in regions of interest selection due to spatial distortion
problems causing discrepancies between DWIs and conventional MRIs. The analysis
of images and ADC values was performed by expert neuroradiologists (Kee-Hyun
Chang, MD, PhD, Department of Radiology, Seoul National University Hospital)
and neurologists (K.C. and D.-W.K.). Perfusion-weighted MRI was not performed.
PATIENT 1
A 61-year-old woman was admitted to the hospital for altered consciousness.
Before admission, nausea, recurrent vomiting, abdominal pain, and swelling
developed gradually for 2 months. Because of the recurrent vomiting, she did
not eat her meals regularly and followed a light liquid diet during the past
2 months. One month before hospital admission, she visited the local clinic,
and mild paralytic ileus was noted. Four days before admission, altered consciousness
and confusion developed. She spoke incomprehensible words to her family and
could not stand without assistance. Her level of consciousness declined, and
on the day of hospital admission she was comatose. The patient was afebrile
and acyanotic. She had a history of ischemic stroke in the left anterior cerebral
artery territory 1 year previously; however, she had since enjoyed good health.
She had hypertension for 2 years and took her medications before the incident.
She had undergone hysterectomy 5 years previously.
In the emergency department she did not respond to painful stimuli.
Vital signs, electrocardiographic evidence, and laboratory findings, including
arterial blood gas values, were normal. Neurologic examination revealed complete
ophthalmoplegia and a slightly rigid neck. Brain MRI, including DWI, and gadolinium
enhancement were performed on the second hospital day (Figure 1). With the help of MRI findings, WE was strongly suspected,
and 200 mg of thiamine was given daily via intravenous and oral routes. On
the fourth hospital day she regained consciousness, and the ophthalmoplegia
started to improve. On the seventh hospital day she became alert and could
communicate with her family. On hospital day 10, the ophthalmoplegia completely
resolved, and mild confabulation was noted. On hospital day 14, follow-up
MRI (Figure 2) showed complete resolution
of the previous high SIs. However, moderate confabulation, attentional deficit,
and gait ataxia remained on hospital day 60.
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Figure 1. Initial magnetic resonance imaging
findings in patient 1. T2-weighted images show the high signal intensities
in the bilateral paramedian thalami with mamillary bodies (A) and in the periaqueductal
gray matter (B). Diffusion-weighted images show the bright high signal intensities
in the corresponding lesions (C and D). The corresponding apparent diffusion
coefficient values of the lesions range from 512 to 545 x 10-6mm2/s.
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Figure 2. Follow-up magnetic resonance imaging
finding in patient 1. T2-weighted images (A and B) and diffusion-weighted
images (C and D) show complete resolution of the lesions in 2 weeks.
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PATIENT 2
A 73-year-old man was admitted to the hospital because of gait disturbance
and diplopia. Nausea, vomiting, and poor oral intake developed 3 weeks before
admission. Because of the severe nausea, he could not eat his meals regularly,
and he ate a light fluid diet. Two weeks before hospital admission, gait disturbance
and diplopia developed, and he could not walk without assistance. The symptoms
progressed, and mental confusion developed 1 week before hospital admission.
He had had rectal cancer and had undergone hemicolectomy with colostomy 5
years earlier. Vital signs, electrocardiographic evidence, and laboratory
findings, including arterial blood gas values, were normal. In the emergency
department, neurologic examination showed confused mentality, left-sided sixth
nerve palsy, and bilateral limb ataxia. Magnetic resonance imaging, including
T1-weighted, T2-weighted, and FLAIR images, was performed with DWI on the
first hospital day. The diagnosis of WE was made using the typical clinical
manifestations and MRI findings, and 200 mg of thiamine was given intravenously
daily. The ataxia and ophthalmoplegia started to resolve on hospital day 2,
and on the fifth hospital day, confused mentality and the previously described
symptoms completely resolved. However, mild confabulation developed on the
seventh hospital day, and the symptoms persisted on hospital day 30.
RESULTS
For patient 1, T2-weighted and FLAIR MRI performed on hospital day 2
showed high SIs in the paramedian thalamus, periaqueductal gray matter, and
mamillary bodies bilaterally (Figure 1A-B).
Diffusion-weighted imaging performed on the same day showed the high SIs in
the corresponding regions (Figure 1C-D).
The ADC values in the corresponding areas were low (512-545 x 10-6mm2/s). Gadolinium enhancement showed no abnormalities.
T1-weighted MRI and MRI angiography showed normal results. In the 2-week follow-up
DWI and T2-weighted images (Figure 2),
the hyperintensities previously seen on DWI were reversed, and the ADC values
were also normalized (876-940 x 10-6mm2/s).
For patient 2, T2-weighted and FLAIR MRI performed on the first hospital
day showed high SIs on the bilateral paramedian thalamus and periaqueductal
gray matter (data not shown). Diffusion-weighted imaging performed on the
same day showed high SIs on the corresponding areas, and the ADC values ranged
from 576 to 612 x 10-6mm2/s. On follow-up
DWI, FLAIR images performed on hospital day 10 showed normal results.
COMMENT
Our patients had WE. The triad of WE symptoms—confusion, ophthalmoplegia,
and gait ataxia—and the typical MRI findings developed during the prolonged
fasting and recurrent vomiting. The neurologic deficits with MRI abnormalities
were improved by administration of thiamine. Findings from DWI in our patients
include reversible high SI in the bilateral paramedian thalamus and periaqueductal
gray matter with decreased ADC values. The findings suggest that the MRI abnormalities
of WE are caused by the cytotoxic edema and can be reversed with adequate
treatment.
The exact mechanisms underlying the pathogenesis of the lesions in WE
are incompletely understood. Vitamin B1 is required as a coenzyme
at intermediate points in carbohydrate metabolism and is important in maintaining
osmotic gradients across cell membranes.19
Thus, vitamin B1 deficiency is associated with intracellular and
extracellular edema. The edema can progress to cellular proliferation, demyelination,
and petechial hemorrhage, leading to cellular degeneration. GlutamateN-methyl-D-aspartate (NMDA) receptor–mediated excitotoxicity has
been proposed as a cause of neuronal cell death in pyrithiamine-induced thiamine
deficiency (PTD) (the animal model of human WE) in rats on the basis of findings
from histologic studies, microdialysis, and enzymatic studies.20-23
Decreased activity of the thiamine-dependent enzyme 2-oxo-glutarate dehydrogenase
is associated with the onset of neurologic signs and the progress of vitamin
B1 deficiency and could lead to the accumulation of glutamate in
the brain.24-26
The characteristic features of neuronal death in PTD are consistent with those
of excitotoxic cell death triggered by glutamate.21, 27-28
The strongest evidence in support of a glutamateNMDA receptor–mediated
process in PTD is that MK 801 (a glutamateNMDA receptor antagonist)
administered to PTD rats blocked the localized increases in extracellular
glutamate concentration in the brain and also significantly attenuated neuronal
cell death.23, 29 Zimitat and Nixon30 suggested a unifying hypothesis for the glutamateNMDA receptor–mediated process in PTD rats. A decrease in 2-oxo-glutarate
dehydrogenase activity could lead to the accumulation of intracellular glutamate
and could adversely affect cellular energy levels in the PTD rat brain, limiting
the function of adenosine triphosphate–dependent pumps of neurons or
glial cells.31 Failure to maintain cellular
electrolyte homeostasis could activate selling-induced anion transporters
on glial cell plasma membranes and the release of intracellular glutamate.32 Increases in extracellular fluid glutamate concentration
and disruption of the glutamate/glutamine cycle could also result from failure
of glutamate transporters on glial cells.33
As vitamin B1 deficiency progresses and 2-oxo-glutarate dehydrogenase
activity and cellular energy reserves further decline, the extracellular fluid
glutamate concentration in affected brain structures could increase, as has
been measured in the thalamus of PTD rats.22-23
Increased extracellular fluid concentrations of glutamate would lead to glutamateNMDA receptor stimulation and thus increased expression of Fos proteins,
which would eventually cause cell death.30
High SIs on DWI and decreased ADC values indicate the presence of cytotoxic
edema, which conventional MRI cannot differentiate. Cytotoxic edema, presented
as high SI on DWI, can occur in various situations, such as acute arterial
infarction,1-9
status epilepticus,34 and WE. The initial triggering
factors leading to cytotoxic edema may also vary according to the main conditions;
however, the subsequent results may become similar, leading to cell death.
In arterial ischemia, the cessation of blood flow can cause the initiation
of ischemic cascade of cell death. In status epilepticus, the main mechanisms
are neuronal hyperexcitability and the excessive release of excitatory amino
acids, such as glutamate.35 In WE, the main
triggering mechanism may be the excitotoxicity caused by the nutritional deficit
(thiamine), affecting glucose metabolism, leading to glutamateNMDA
receptor–mediated excitotoxicity. Questions about the reversibility
of affected tissue might arise. The high SIs on DWI do not always indicate
irreversibility but the presence of "tissue at risk." Dardzinski et al36 reported ADC changes over time after permanent middle
cerebral artery occlusion.
They suggested the following ADC values: (1) at
less than 450 x 10-6mm2/s, severe ischemia
and irreversible damage occur; (2) at greater than 550 x
10-6mm2/s, infarction does not occur; and (3) at 450 to 550 x
10-6mm2/s, the damage is potentially reversible.
Our ADC results (patient 1: 512-545 x 10-6mm2/s; patient 2: 576-612 x 10-6mm2/s)
corresponded well with those of the previous studies. With adequate treatment,
the DWI abnormalities in WE might be reversible, similar to the cells in the
ischemic penumbra.36-38
Abnormalities on DWI in our patients indicate that MRI abnormalities
in WE might be due to cytotoxic edema caused by vitamin B1 deficiency.
Our findings suggest that DWI can be used as a tool in researching the pathogenesis
of WE and in predicting the outcome of tissue with adequate treatment.
AUTHOR INFORMATION
Accepted for publication August 28, 2001.
Author Contributions: Study concept and
design (Drs Chu, Kang, Kim, Lee, and Park); acquisition of data (Drs Chu, Kang, Kim, Lee, and Park); analysis and interpretation
of data (Drs Chu, Kang, Kim, and Park); drafting of the manuscript (Drs Chu, Kang, Kim, Lee, and Park); critical revision of the
manuscript for important intellectual content (Drs Chu, Kang, Kim,
Lee, and Park); statistical expertise (Dr Kim); obtained
funding (Dr Kim); administrative, technical, and material support (Drs Chu, Kang, Kim, and Park); and study supervision
(Drs Kim and Lee).
This work was supported by the clinical research fund of Seoul Boramae
Municipal Hospital, Seoul, Korea.
We thank Yon-Jae Chung, BSc(Pharm), MS, for her editorial assistance.
Corresponding author and reprints: Seong-Ho Park, MD, PhD, Department
of Neurology, Seoul Boramae Municipal Hospital, 395, Shindaebang 2-Dong, Dongjak-Gu,
Seoul 156-012, Korea (e-mail: nrpsh{at}brm.co.kr).
From the Department of Neurology and Clinical Research Institute, Seoul
National University Hospital, Neuroscience Research Institute of Seoul National
University Medical Research Center (Drs Chu, Kang, and Kim), and the Department
of Neurology, Seoul Boramae Municipal Hospital (Drs Lee and Park), Seoul,
Korea; and Section on Stroke Diagnostics and Therapeutics, National Institute
of Neurological Disorders and Stroke (Dr Kang), Bethesda, Md.
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