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Diffusion-Weighted and Gradient Echo Magnetic Resonance Findings of Hemichorea-Hemiballismus Associated With Diabetic Hyperglycemia
A Hyperviscosity Syndrome?
Kon Chu, MD;
Dong-Wha Kang, MD, PhD;
Dong-Eog Kim, MD;
Seong-Ho Park, MD, PhD;
Jae-Kyu Roh, MD, PhD
Arch Neurol. 2002;59:448-452.
ABSTRACT
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Background The magnetic resonance (MR) imaging findings of hemichorea-hemiballismus
(HCHB) associated with hyperglycemia are characterized by hyperintensities
in the striatum on T1-weighted MR images and computed tomographic scans, with
a mechanism of petechial hemorrhage considered to be responsible. Diffusion-weighted
MR imaging (DWI) has been reported to detect early ischemic damage (cytotoxic
edema) as bright areas of high signal intensity and vasogenic edema as areas
of heterogeneous signal intensity. We report various DWI findings in 2 patients
with hyperglycemic HCHB.
Objectives To describe the DWI and gradient echo findings and characterize the
types of edema in HCHB associated with hyperglycemia.
Setting A tertiary referral center neurology department.
Design and Methods Two patients with HCHB associated with hyperglycemia underwent DWI,
gradient echo imaging, and conventional MR imaging with gadolinium enhancement.
The patients had an elevated serum glucose level on admission and a long history
of uncontrolled diabetes, and the symptoms were controlled by dopamine receptor
blocking agents. Initial DWIs were obtained 5 to 20 days after symptom onset.
Apparent diffusion coefficient (ADC) values were measured in the abnormal
lesions with visual inspection of DWI and T2-weighted echo planar images.
Results T1- and T2-weighted MR images and brain computed tomographic scans showed
high signal intensities in the right head of the caudate nucleus and the putamen.
Gradient echo images were normal. The DWIs showed bright high signal intensity
in the corresponding lesions (patient 1), and the ADC values were decreased.
The decrease in ADC and the high signal intensity on DWI persisted despite
the disappearance of HCHB, even after 70 days.
Conclusions Gradient echo MR imaging findings were normal in HCHB with hyperglycemia,
whereas DWI and the ADC map showed restricted diffusion, which suggests that
hyperviscosity, not petechial hemorrhage, with cytotoxic edema can cause the
observed MR abnormalities.
INTRODUCTION
HEMICHOREA-HEMIBALLISMUS (HCHB) is usually continuous, nonpatterned,
involuntary, and associated with stroke, and infrequently associated with
infections, drug usage, metabolic derangement, neurodegenerative disorder,
tumors, and hyperglycemia.1 A few cases of
HCHB with hyperglycemia have been reported.2-9
Since the significant association between hyperglycemia and striatal hyperintensity
on T1-weighted magnetic resonance (MR) images in HCHB was pointed out, much
attention has been focused on the mechanism of HCHB, and petechial hemorrhage
with blood-brain barrier breakdown in the striatum has been suggested as the
most plausible mechanism.2-4
Two cases of HCHB with hyperglycemia and MR imaging findings, including
diffusion-weighted imaging (DWI) and gradient echo imaging (GE), are reported
herein. Our findings suggest that mechanisms other than the petechial hemorrhage
do in fact exist.
PATIENTS AND METHODS
CLINICAL HISTORY
Patient 1
A 69-year-old woman was admitted for sudden onset of abnormal movement
on the left side. Three days before admission, hemichorea had developed suddenly,
and the intensity had aggravated during these 3 days. She had no hemiparesis,
sensory deficits, or any other neurologic deficits. She had a history of diabetes
mellitus for 7 years and took an oral hypoglycemic agent irregularly. She
had no history of hypertension, headache, parkinsonism, or other neurologic
diseases. At admission, the initial blood glucose level was 348 mg/dL (19.3
mmol/L) and hemoglobin A1c concentration was 9.5%. Neurologic examination
showed normal findings except for the hemichorea in the left side. Brain computed
tomography was performed on the first hospital day (Figure 1A). Brain MR imaging, including DWI, GE, and T1- and T2-weighted
images with gadolinium enhancement, was performed on the second hospital day
(Figure 1B-F). The chorea was controlled
with risperidone (4 mg/d) after 14 days. Serum glucose level was maintained
within the therapeutic ranges by insulin. The patient was discharged with
no specific symptoms on the 30th hospital day. Follow-up GE and T1- and T2-weighted
MR imaging was performed on the 14th hospital day and 70 days after onset
(not shown). On the 120th day after onset, risperidone was discontinued, and
chorea had not reappeared by the 190th day.
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Figure 1. A, Brain computed tomographic
scan of patient 1, performed on the third day after hemichorea onset, showing
high-attenuated areas in the right striatum. B-E, Brain magnetic resonance
images, obtained on the next day, showing high signal intensities in the caudate
nucleus head and putamen on T1-weighted image (B) and focal high signal intensity
in the putamen on T2-weighted (C) and diffusion-weighted (E) images. Gradient
echo image shows normal findings (D). F, Apparent diffusion coefficient map
shows the corresponding areas as low signal intensities. The respective apparent
diffusion coefficient values of the lesions are as follows: 1 (core), 419
x 10-6 to 432 x 10-6 mm2/s; 2 (surrounding areas), 519 x 10-6 to 597
x 10-6 mm2/s; 3 and 4 (contralateral normal
areas), 812 x 10-6 to 896 x 10-6
mm2/s.
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Patient 2
A 62-year-old woman was admitted for sudden onset of choreatic movement
on the left side. Twenty days before admission, hemichorea had developed suddenly.
The intensity of the symptoms had increased during this period. She had had
poorly controlled diabetes mellitus for 2 years. The hemoglobin A1c
concentration was 9.7%, and initial blood glucose level was 370 mg/dL (20.5
mmol/L) at admission. Neurologic examination showed normal findings except
for the left hemichorea. Brain MR imaging, including DWI, GE, and T1- and
T2-weighted images, was performed on the 22nd day after the onset of symptoms
(Figure 2). Serum glucose level
was maintained within the therapeutic ranges by insulin. Hemichorea was controlled
with oral haloperidol (4 mg/d), and the patient was discharged on the 10th
hospital day with no specific symptoms. Haloperidol was stopped on the 70th
day after onset, and chorea had not reappeared by the 120th day after onset.
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Figure 2. Brain magnetic resonance images
of patient 2, obtained on the 21st day after hemichorea onset, showing normal
diffusion-weighted (A) and gradient echo (B) findings. The T1-weighted image
(C) shows high signal intensity in the right putamen. The apparent diffusion
coefficient values of the corresponding lesions are 650 x 10-6 to 695 x 10-6 mm2/s.
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DATA ACQUISITION AND ANALYSIS
The patients were examined by the same MR imaging protocol used in our
previous studies.10-13
The patients were examined with a 1.5-T MR unit (Signa Horizon, Echospeed;
General Electric Medical Systems, Milwaukee, Wis) with echo planar imaging
capability. Fast spin-echo, T2-weighted images (repetition time/echo time,
4200/112 milliseconds; field of view, 21x21 cm; matrix, 256x192;
and slice thickness, 5 mm with 1.5-mm gap) and T2*-weighted GE sequences (repetition
time/echo time, 200-500/15 milliseconds; flip angle, 20°; number of excitations,
2; slice thickness, 1.4 mm; gap width, 0.7 mm) were obtained. The DWIs were
obtained in the transverse plane by means of a single-shot echo planar image
(repetition time/echo time, 6500/125 milliseconds; field of view, 24x24
cm; matrix, 128x128; slice thickness, 5 mm with 2.5-mm gap; and 2 b values, 0 and 1000 s/mm2). The diffusion gradients
were applied along 3 axes (x, y, z) simultaneously. The apparent diffusion
coefficient (ADC) was calculated on the basis of the Stejskal-Tanner equation
as the negative slope of the linear regression line best fitting the points
for b vs ln(SI), where ln
represents natural log and 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. Normal ADC values of the parenchyma and white matter range from
0.78x10-3 to 0.91x10-3 mm2/s (K.C., D.-W.K., unpublished data, 2000).11-13
The ADC values are uniform throughout the brain and not intrinsically lower
in specific areas. Regions of interest were carefully drawn in the abnormal
areas on calculated average ADC maps, as well as in normal-appearing areas.
The region of interest (25 mm2) was selected with the help of T2-weighted
echo planar images of the same acquisition as the diffusion images (ie, images
generated from the diffusion sequence with diffusion sensitivity b = 0) to avoid errors in selection of region of interest due to spatial
distortion problems causing discrepancies between diffusion images and conventional
MR images.
RESULTS
The brain MR image of patient 1, performed on the fourth day after onset,
showed high signal intensities in the right head of the caudate nucleus, the
globus pallidus, and the putamen on T1-weighted images, which spared the anterior
limb of the internal capsule, and focal high signal intensity on T2-weighted
MR images and DWI (Figure 1B, Figure 1C, Figure 1E). Gadolinium-enhanced T1-weighted images showed no abnormal
enhancement, and GE also displayed no abnormal findings (Figure 1D). The ADC map presented low signal intensities and low
ADC values (419 x 10-6 to 432 x 10-6 mm2/s) in the corresponding lesions (Figure 1F). The ADC values of the surrounding lesions were 519 x
10-6 to 597 x 10-6 mm2/s,
while those of the contralateral side were normal (812 x 10-6 to 896 x 10-6 mm2/s). Brain computed
tomography, performed on the third day after onset, showed high-attenuated
areas in the same lesions (Figure 1A).
Follow-up MR imaging, performed 17 and 70 days after onset, showed similar
findings with no significant interval change of ADC values (not shown).
The brain MR images of patient 2, performed on the 21st day after onset
of symptoms, showed high signal intensities in the right striatum on T1-weighted
MR images (Figure 2A). The T2-weighted
MR images showed low to mild high signal intensities in the corresponding
lesions (not shown). The DWI and GE presented normal findings (Figure 2B and Figure 2C),
and the ADC map showed decreased ADC values in the corresponding lesions (650
x 10-6 to 695 x 10-6 mm2/s) compared with the contralateral side (854 x 10-6 to 912 x 10-6 mm2/s).
COMMENT
Our 2 patients had hemichorea associated with hyperglycemia. The DWI
findings showed restricted diffusion in both patients and bright high signal
intensity on DWI in patient 1. There was no evidence of petechial hemorrhage
on GE images. The DWI and ADC map of patient 1 displayed low ADC values in
surrounding areas as well as T1 hyperintensity lesions. The ADC values were
as low as in acute arterial ischemia, being the lowest (419 x 10-6 to 432 x 10-6 mm2/s) in the
focal high-signal-intensity lesion on T1- and T2-weighted MR images and DWI.
The surrounding areas showed T1–high density, T2-isodense, and DWI-isodense
lesions with low ADC values (519 x 10-6 to 597 x
10-6 mm2/s). The brain MR image of patient 2 displayed
high signal intensities on T1-weighted images with normal DWI and GE findings.
The ADC values of the corresponding area were slightly decreased. The time
from onset to MR imaging was variable, ranging from 4 to 21 days, which implied
that different MR imaging stages could occur.
The critical pathophysiology of HCHB associated with hyperglycemia is
unknown. Hyperglycemia can disrupt the blood-brain barrier and produce a global
decrease in regional cerebral blood flow, intracellular acidosis, accumulation
of extracellular glutamate, brain edema formation, and decreased activity
of  -aminobutyric acid–enkephalin inhibitory neurons.4, 14-15 The decreased -aminobutyric
acid activity due to its metabolism as an alternate energy substrate during
hyperglycemic crisis has been proposed. The fact that the chorea may persist
well beyond the episode of hyperglycemia argues against this mechanism.9 In addition, the MR imaging abnormalities, including
high signal intensities on computed tomography and T1-weighted MR imaging,
cannot be explained. The nature of the characteristic MR signal changes associated
with HCHB has been the subject of considerable controversy. Petechial hemorrhage,2-4 myelinolysis,5 and calcifications6
have been suggested as possible mechanisms. Petechial hemorrhage with blood-brain
barrier breakdown in the striatum has been suggested as the most plausible
mechanism.
However, the GE findings presented here suggest that petechial hemorrhage
cannot be responsible for the lesions. Recently, a salient autopsy report
of HCHB was published.16 The main findings
included multiple infarcts associated with reactive astrocytic and interneuronal
response, not with petechial hemorrhage and calcification.16
Shan et al7 hypothesized that the possible
cause of the MR imaging abnormalities might be the mild ischemia with gemistocyte
accumulation, and they described one patient whose biopsy specimen showed
gliotic brain tissue with abundant gemistocytes.7
Gemistocytes are swollen reactive astrocytes, containing a rich protein content,
that usually appear during acute injury but later gradually shrink. Shortening
of T1 relaxation time can result from the protein hydration layer inside the
cytoplasm of swollen gemistocytes, as in a reported case of gemistocytic astrocytoma.17-18 The T1 relaxation time depends on
the movement of molecules, and the rich protein content causes electrostatic
forces that restrict the motion of water molecules, which may explain the
DWI abnormalities of patient 1 in the surrounding lesions with low ADC values.
The core lesion on DWI might result from transient, mild ischemia due to high
viscosity and decreased perfusion. The MR image of patient 2 showed the subacute
findings of HCHB. The DWI and T2-weighted MR image began to be normalized,
but the abnormalities on T1-weighted MR images remained. The ADC values of
patient 2 were slightly lower despite the normal DWI, and T2-weighted MR images
showed low to normal signal intensities in the corresponding lesions. In DWI,
high-amplitude bipolar gradients sensitize a T2-weighted MR image to the brownian
motion of water molecules. Despite the small magnitude of motion during diffusion
gradient, it results in intravoxel dephasing and signal loss.19
Signal intensity on DWI is thus due to 2 intrinsic competing components: degree
of T2 signal intensity and degree of diffusion. Provenzale et al19
have shown normal DWI findings despite significant vasogenic edema in posterior
reversible encephalopathy syndrome. They term this phenomenon T2 washout, since the intravoxel dephasing related to the increased
water diffusion in the vasogenic edema washes out the inherent increased T2
signal intensity in the lesions.19-20
A T2 shortening in HCHB has been well known with T1 shortening.8-9
The T2 washout effect can be applied in the normal DWI findings of patient
2, since decreased water diffusion in the hyperviscous striatum may wash out
the decreased T2 signal intensity in the corresponding lesions.
The restricted diffusion of water (low ADC values) has been reported
in various diseases, such as acute stroke,10
Wernicke encephalopathy,13 epidermoid mass,18 brain abscess,21 and
status epilepticus.11 The proposed mechanisms
of ADC decrease, which are still being discussed, address changes in the diffusion
characteristics of the intracellular and extracellular water compartments,
including restricted diffusion, water exchange across permeable boundaries,
the concept of extracellular tortuosity, and the intracellular and extracellular
volume fraction.22 In addition, while the initial
triggering factors leading to restricted diffusion may vary according to the
main conditions, the subsequent results may be similar, leading to cell death.
In arterial ischemia,10 the cessation of blood
flow can cause initiation of the ischemic cascade of cell death. In status
epilepticus,11 the primary mechanisms are neuronal
hyperexcitability and the excessive release of excitatory amino acids, such
as glutamate. In brain abscess and high-cellularity tumor, hyperviscosity
can be the probable mechanism of restricted diffusion.18, 20
Shan and coworkers' results7 and our DWI findings
suggest that hyperviscosity can be responsible for the restricted diffusion
in HCHB caused by hyperglycemia, which can cause the partial neuronal death
and dysfunction on the vulnerable striatum, similar to the partial ischemic
injury model,23 in predisposed individuals.
The MR imaging abnormalities in HCHB are often reversible, but the mechanisms
of such abnormalities are unknown. We suggest that the ADC threshold values
might play a role in determining the "tissue fate." Dardzinski et al24 reported the ADC changes over time after permanent
occlusion of the middle cerebral artery and suggested the following ranges
of ADC values: (1) less than 450 x 10-6 mm2/s:
severe ischemia and irreversible damage occur; (2) greater than 550 x
10-6 mm2/s: infarction will not occur; (3) 450
x 10-6 to 550 x 10-6 mm2/s: potentially reversible. Our results (ADC values of patient 1: core,
419 x 10-6 to 432 x 10-6 mm2/s; surrounding areas, 519 x 10-6 to 597 x
10-6 mm2/s; patient 2: 650 x 10-6 to 695 x 10-6 mm2/s) corresponded
well to the previous reports and hence suggest that, with adequate treatment,
the DWI abnormalities (cytotoxic edema) might be reversible, as with the cells
in the ischemic penumbra.13
The DWI and GE MR imaging findings in HCHB associated with hyperglycemia
suggest that gemistocyte accumulation, hyperviscosity, neuronal dysfunction,
and possible cytotoxic edema can cause the observed MR imaging abnormalities
in possible susceptible individuals. Diffusion-weighted imaging can be used
in determining the tissue fate with the analysis of ADC values.
AUTHOR INFORMATION
Accepted for publication November 6, 2001.
Author contributions: Study
concept and design (Drs Chu, Kang, Kim, Park, and Roh); acquisition of data (Drs Chu, Kang, and Roh); analysis
and interpretation of data (Drs Chu, Kang, Kim, Park, and Roh); drafting of the manuscript (Drs Chu, Kang, and Roh); critical revision of the manuscript for important intellectual
content (Drs Chu, Kang, Kim, Park, and Roh); administrative,
technical, and material support (Dr Chu); study supervision (Drs Kang, Kim, Park, and Roh).
Corresponding author and reprints: Jae-Kyu Roh, MD, PhD, Department
of Neurology, Seoul National University Hospital, 28, Yongon-Dong, Chongro-Gu,
Seoul 110-744, South Korea (e-mail: rohjk{at}snu.ac.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, Kim, and Roh), and Department
of Neurology, Seoul Boramae Municipal Hospital (Dr Park), Seoul, South Korea;
and Section on Stroke Diagnostics and Therapeutics, National Institute of
Neurological Disorders and Stroke, Bethesda, Md (Dr Kang).
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