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Correlation of Diffusion-Weighted Magnetic Resonance Imaging With Neuropathology in Creutzfeldt-Jakob Disease
Sanjay Mittal, MD;
Peter Farmer, MD;
Peter Kalina, MD;
Peter B. Kingsley, PhD;
John Halperin, MD
Arch Neurol. 2002;59:128-134.
ABSTRACT
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Background Although the diagnosis of Creutzfeld-Jakob disease (CJD) is straightforward
in fully developed cases, a definitive diagnosis can be difficult early in
the course of the illness. T2-weighted magnetic resonance imaging (MRI) signal
abnormalities, and recently, diffusion-weighted MRI abnormalities, have been
described in patients with CJD, suggesting the utility of MRI in the early
recognition of CJD.
Objective To correlate diffusion-weighted MRI signal abnormalities with neuropathologic
changes in CJD.
Materials and Methods Diffusion-weighted MRI and neuropathologic changes of 2 patients with
autopsy-proven CJD were examined in a blinded fashion by a neuroradiologist
and a neuropathologist.
Results Areas of bright signal on diffusion-weighted MRI correlated with a higher
degree of spongiform changes.
Conclusion Diffusion-weighted MRI in CJD demonstrates specific-signal abnormalities
that correlate well with areas of the most severe and characteristic neuropathologic
changes.
INTRODUCTION
CREUTZFELDT-Jakob disease (CJD) is a fatal prion-mediated neurodegenerative
illness characterized by rapidly progressive dementia, a cerebellar-extrapyramidal
syndrome, diffuse myoclonus, and periodic discharges on electroencephalography.
Progress in our understanding of this group of disorders continues at a prodigious
rate although the definitive confirmation of symptomatic prion disease still
requires pathologic examination, most reliably performed post mortem.1
Immunoassay for cerebrospinal fluid protein 14-3-3 is a useful biochemical
marker for CJD. Its positive predictive value varies in different clinical
settings, and it may be detectable in other neurodestructive processes.2 Computed tomographic examination in patients with
CJD may demonstrate atrophy,3 as does the gross
appearance of the brain in advanced cases.
Increased T2-weighted and diffusion-weighted (DW) magnetic resonance
imaging (MRI) signal has been described in the basal ganglia of subjects with
sporadic CJD. Abnormal fluid-attenuated inversion recovery4
and T2-weighted5 images on MRI have also been
reported in the thalamus (pulvinar sign) of patients with variant CJD. Variant
CJD is a disease characterized by onset in a younger age group, early neuropsychiatric
features, and the occurrence of prominent sensory symptoms with neurologic
signs such as ataxia and involuntary movements later in the course of the
disease.6
We describe 2 patients with autopsy-proven CJD who had abnormal DW MRIs
early in the course of their illness. The areas of specific signal abnormalities
in both patients correlated with the neuropathologic findings of spongiform
encephalopathy.
REPORT OF CASES
PATIENT 1
Over the course of 5 weeks, this 65-year-old, right-handed man developed
progressive forgetfulness, social withdrawal, gait disturbance, and decreased
speech. His father died of CJD 23 years earlier. Findings from the physical
examination disclosed dysphasia, bilateral extrapyramidal signs, and widespread
resting, action, and startle myoclonus.
The results of the biochemical and hematologic profiles were normal.
Noncontrast computed tomographic and routine MRI scans of the head showed
no abnormalities. Electroencephalography showed diffuse slowing with triphasic
waves. Cerebrospinal fluid was negative for protein 14-3-3. Genetic studies
demonstrated GAG (glutamine) to AAG (lysine) substitution at codon 200 and
M/M (methionine/methionine) homozygosity at codon 129 of the PRNP gene. The DW MRIs disclosed specific signal abnormalities. The
patient died 4 weeks later.
PATIENT 2
Over the course of 4 weeks this 56-year-old, left-handed woman developed
memory difficulty, blurred vision, and progressive gait unsteadiness. Limb
and truncal ataxia was noted on neurologic examination. Generalized and startle
myoclonus became apparent during the course of her hospitalization. Results
of the biochemical and hematologic profiles were normal.
Her initial noncontrast cranial computed tomographic and MRI scans showed
no abnormalities. Electroencephalograpy demonstrated diffuse slowing with
triphasic waves. Cerebrospinal fluid was negative for protein 14-3-3. The
DW MRIs showed specific signal abnormalities. The patient died about 5 weeks
after being discharged from the hospital.
SUBJECTS, MATERIALS, AND METHODS
Magnetic resonance imaging data were acquired on a 1.5-T scanner (General
Electric Medical Systems, Milwaukee, Wis), including T1-weighted and fast
spin-echo T2-weighted images. The DW imaging was performed with contiguous
slices 3.3 mm thick and a b-factor of 1000 s/mm2 along 1 of 3 orthogonal
axes (x, y, or z). A set of T2-weighted images was acquired in an identical
manner except that the b-factor was 5 s/mm2. From the 3 DW images
an average DW image was derived automatically as the geometric mean of the
individual signal intensities (SIs) in each pixel: SI (DW) = [SIx
x SIy x SIz]1/3. The apparent
diffusion coefficient (ADC) was calculated for each pixel in these images
from the formula7: ADC (m2/s) =
ln[SI(T2)/SI(DW)]/(1000 - 5). The apparent diffusion coefficient values
are multiplied by 106 for presentation, so the final ADC values
have units of 10-6mm2/s. This ADC calculation
is equivalent to averaging the ADCs measured from the separate x, y, and z
DWIs, ADC = (ADCx + ADCy + ADCz)/3.
Pixels for calculation of the mean ADC were chosen from the areas of
signal abnormality on the DW images. At least 3 regions of interest with an
SD less than 30% were selected on multiple contiguous slices for each area
of abnormal signal. Three or more ADC values were averaged to obtain a mean
ADC for each anatomical area.
The brain was obtained post mortem and fixed in 10% neutral-buffered
formalin. Tissue blocks from the first case were obtained from the left occipital
parasagittal cortex and bilateral temporal poles, thalamus, striatum, and
parasagittal frontal and parietal cortex. Tissue blocks from the cerebellum
and right occipital parasagittal cortex were unavailable. In the second case,
the entire right cerebral hemisphere was frozen for biochemical studies; tissue
blocks were sampled from the left thalamus; basal ganglia; frontal, temporal,
and occipital cortex; and cerebellum.
Tissue was embedded in paraffin, sectioned at 6 µm, stained with
hematoxylin-eosin, and examined by light microscopy. A neuropathologist (P.F.)
who was blinded to the MRI results examined all of the slides. A score for
each region of interest was derived based on an overall score from the multiple
fields examined.
Observations were made independently for each of the following 4 measures:
the cytoarchitectural integrity of that region, degree of neuronal loss, degree
of spongiform change, and reactive astrocytosis. A score of 0 to 3 was assigned
to each measure. For each variable grade 0 represented the absence of any
significant pathologic changes. Grade 1 represented mild spongiform change
with early vacuolar degeneration in the neuropil and neurons; cytoarchitecture
mildly disrupted; and astroglial nuclei increased in number and size. Grade
2 represented extensive spongiform change with focal confluence of vacuoles;
cortical cytoarchitecture disrupted with loss of polarity of neurons and some
depletion of nerve cells; and clear proliferation of fibrillar astrocytes.
Grade 3 represented severe spongiform change with extensive confluence of
vacuoles; severe disruption of cortical architecture with prominent neuronal
loss; and extensive glial proliferation. A possible minimum of 0 and a maximum
score of 12 thus generated was used to define and compare the varying degrees
of pathologic changes in the different regions of interest.
Corresponding neuropathologic and MRI data were available for 17 regions
of interest. All variables were compared statistically (Statview 5.0.1 for
Macintosh; SAS Institute, Cary, NC). The (ordinal) neuropathologic variables
were correlated with corresponding ADC values using the Spearman rank correlation
and to the dichotomous qualitative variable (presence or absence of DW MRI
changes) using the Mann-Whitney test.
RESULTS
RADIOLOGICAL EXAMINATION
Case 1
T1-weighted MRIs showed mild sulcal prominence. The T2-weighted
fast spin-echo sequences (Figure 1)
revealed abnormal increased signal bilaterally in the corpus striatum (Figure 1C). The DW signal abnormality in
the bilateral corpus striatum appeared much more prominent than the T2-weighted
abnormality (Figure 1D). The DW
MRIs showed increased signal in the deep cortical layers of the left temporal
lobe extending to the perisylvian region and in the bilateral parasagittal
frontal, parietal, and occipital cortex as well as the left frontal cortex
(Figure 1B). These regions did not
appear hyperintense on T2-weighted images (Figure 1A). Bright DW MRI signals corresponded with restricted diffusion
(low ADC values), most notably in both basal ganglia (right basal ganglia
ADC = 417 x 10-6mm2/s, left basal
ganglia ADC = 457 x 10-6mm2/s)
and the left temporal lobe (635 x 10-6mm2/s).
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Figure 1. Case 1. Axial magnetic resonance
images. T2-weighted image through the temporal lobes (A) demonstrates no signal
abnormality while the diffusion-weighted image (B) demonstrates increased
signal in the left temporal cortex. T2-weighted image (C) demonstrates mildly
increased signal in the basal ganglia while diffusion-weighted imaging (D)
demonstrates bright signal in the basal ganglia bilaterally.
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Case 2
T2-weighted images showed slight symmetric hyperintense signal bilaterally
in the putamen and caudate nucleus Figure
2. The DW MRIs showed focal areas of increased signal in the left
putamen but not in the right putamen. The left parietal and superior occipital
lobes showed cortical gyriform hyperintensity, and bilateral frontal parasagittal
areas showed similar features (Figure 2B).
The DW MRIs also showed hyperintensity of theleft cerebellar cortex with sparing
of the deeper nuclear struc tures (Figure
2D). Areas of abnormal signal on the DW MRI indicated restricted
diffusion.
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Figure 2. Case 2. Axial magnetic resonance
images.T2-weighted images through the frontal and parietal lobes (A) and the
cerebellum (C) show no signal abnormality. Corresponding diffusion-weighted
images demonstrate left parietal and bilateral frontal parasagittal cortical
gyriform hyperintensity (B). Diffusion-weighted imaging of the left cerebellum
(D) demonstrates mild signal hyperintensity.
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NEUROPATHOLOGIC EXAMINATION FINDINGS
Case 1
The region of the left temporal lobe corresponding to the abnormal area
on DW MRI showed complete loss of cortical cytoarchitecture and severe spongiform
change with areas of confluent vacuolation, an advanced degree of neuronal
loss, and some reactive astrocytosis (Figure
3A) (Table 1). In the
right temporal lobe, which did not show changes on MRI, spongiform changes
were mild with minimal neuronal loss, no astrocytic reaction, or preservation
of the cortical cytoarchitecture (Figure 3B). Basal ganglia showed marked spongiform degeneration and an advanced
degree of reactive astrocytosis. Varying degrees of spongiform change were
seen throughout the entire brain.
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Figure 3. Case 1. A, Neuropathologic changes
in the left temporal lobe include severe spongiform changes, an advanced degree
of neuronal loss, and obliteration of cytoarchitecture in the cerebral cortex
(hematoxylin-eosin, original magnification x400). B, Neuropathologic
changes of the right temporal lobe include minimal spongiform changes, some
neuronal loss, and preserved cytoarchitecture (hematoxylin-eosin, original
magnification x400).
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Neuropathologic and Magnetic Resonance Imaging Observations in Cases
1 and 2*
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Case 2
The region of the left occipital lobe corresponding to the abnormal
signal on DW MRI showed severe spongiform changes with an advanced degree
of neuronal loss, disrupted cytoarchitecture, and reactive astrocytosis (Figure 4B) (Table 1). Examination of the left cerebellar hemisphere showed a
moderate degree of spongiform changes with neuronal loss and some reactive
astrocytosis (Figure 4A). The frontal
cortex and basal ganglia on the left side showed a moderate degree of spongiform
change with some loss of cytoarchitecture while the neuronal loss and reactive
astrocytosis were minimal. The left thalamus showed areas of minimal change
intermingled with areas of normal-appearing tissue. Findings from the examination
of the left temporal cortex were remarkable for minimal spongiform changes.
No amyloid plaques were present.
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Figure 4. Case 2. A, Neuropathologic changes
in the neuropathologic features of the cerebellar cortex consist of typical
spongiform change in the molecular layer (hematoxylin-eosin, original magnification
x200). B, Neuropathologic changes of the occipital cortex clearly demonstrate
the advanced degree of spongiform change, neuronal loss, and reactive astrocytosis
(hematoxylin-eosin, original magnification x400).
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CORRELATIONS
The 4 different measures of neuropathologic damage all correlated strongly
with each other (Spearman rank correlation; P<.005
for all comparisons). The DW MRI scores correlated strongly (Mann-Whitney
test) with cytoarchitectural loss (P = .003), neuronal
loss (P = .007), and spongiform changes (P = .02), but not astrocytosis (P = .07).
The ADC correlated with cytoarchitectural loss (r2 = 0.56; P<.001), neuronal loss (r2 = 0.75, P<.001),
spongiform changes (r2 = 0.44, P = .01), and astrocytosis (r2
= 0.57, P = .003).
Although the number of data points is small, several general statements
can be made regarding thresholds of the different variables. In general, an
ADC score of 700 or less was associated with a positive DW MRI signal. Moreover,
a positive DW MRI signal was almost always associated with a spongiosis score
of 2 or more or, somewhat less consistently, with a total pathologic score
of 5 or more. Similar correlations with the other pathologic variables appeared
to be less consistent.
COMMENT
A definitive diagnosis of CJD rests on the demonstration of the neuropathologic
triad of neuronal loss, spongiform change, and reactive astrocytosis in the
absence of an inflammatory reaction. When present, amyloid plaques that stain
with  -PrP antibodies are diagnostic of CJD.8
However, these pathologic changes vary considerably from case to case. Spongiform
degeneration of the cortex occurs in virtually all cases regardless of the
clinical presentation and consists of round to oval vacuoles 5 to 25 µm
in diameter located in the neuropil between nerve cell bodies. At times their
presence may be the only neuropathologic clue to the diagnosis of spongiform
encephalopathy. Late-stage disease, recognized as "status-spongiosis" by Masters
and Richardson,9 is characterized by larger
100-µm vacuoles surrounded by a dense meshwork of reactive astrocytic
processes. Though earlier attempts failed to demonstrate parenchymal changes
on MRI,10 in 1988 Gertz et al11
described an increased T2-weighted MRI signal in the basal ganglia of a 55-year-old
woman with proven CJD. Numerous publications since then have consistently
demonstrated bilaterally symmetric, diffuse hyperintense abnormalities in
the basal ganglia on the T2-weighted MRI of patients with CJD.12-13
Recently,5 an increased T2-weighted signal
was described in the thalamus (pulvinar sign) in 28 of 36 patients with variant
CJD. Definite MRI signal changes were also demonstrated in a hamster model
of scrapie.14
Diffusion-weighted MRI is a newer technique that noninvasively images
molecular water proton diffusion processes occurring on a micrometer scale.
The observed proton diffusion rate and direction reflect the molecular and
macromolecular barriers, or hindrances, that the proton experiences during
its translation process.15 This technique,
when used in the demonstration of an acute ichemic infarct, reflects a shift
of relatively faster-translating extracellular water protons into a more hindered
intracellular environment correlating with cytotoxic edema in the acute phase
of an ischemic infarct.
Diffusion-weighted MRIs signal changes encountered in CJD probably are
a result of microvacuolation of neuritic processes heralding spongiform degeneration.
Vacuoles with a diameter of 5 to 20 µm would provide a population of
mobile water molecules with a long T2 yet with a restricted diffusion range.
Diffusion can be visualized by a "diffusion sphere" (or ellipsoid, for asymmetric
diffusion) whose radius R = (2Dt)1/2 is the mean-squared displacement of a particle with
diffusion coefficient D from the center of the sphere
in time t.7 For D = 625 x 10-6mm2/s (typical
for tissues, see Table 1) and t = 80 ms (a typical diffusion time for a DW sequence), R = 10 µm; therefore, a vacuole diameter of less
than about 20 µm would provide restricted diffusion compared with normal
tissue.
Bahn et al16 were able to demonstrate
increased DW MRI signal in the caudate nuclei, putamina, thalami, cingulate
gyri, and right inferior frontal cortex of a patient with proven CJD in whom
the T2-weighted MRIs showed a slightly increased signal in the caudate nucleus
and putamen. Other workers17-18
noted similar observations. Recently Samman et al19
have demonstrated a positive correlation between MRI signal changes and spongiform
degeneration in a 68-year-old patient with CJD.
In our patients, characteristic DW MRI signal abnormalities in the basal
ganglia and deeper cortical layers suggested the diagnosis of CJD early in
the course of their illness, even before the diagnostic abnormalities were
noted on electroencephalograpy or in protein 14-3-3 values. Though T2-weighted
signal abnormalities were also noted in both patients, those abnormalities
were subtle in nature and limited to the basal ganglia. Measurement of ADC
demonstrated restricted diffusion in the areas showing DW MRI changes. This
suggests that restricted diffusion rather than T2 shine-through is specifically
responsible for the signal abnormalities. Regions of increased signal with
DW MRI corresponded to areas of marked spongiform change.
CONCLUSION
Diffusion-weighted magnetic resonance imaging provide a highly sensitive
method of identifying areas of involvement in CJD. This observation may facilitate
the earlier diagnosis of this disease.
AUTHOR INFORMATION
Accepted for publication August 1, 2001.
Author Contributions: Study concept and
design (Drs Mittal, Farmer, and Halperin); acquisition of data (Drs Kalina, Kingsley, and Halperin); analysis and interpretation
of data (Drs Kingsley and Halperin); drafting of the manuscript (Drs Mittal, Farmer, Kingsley, and Halperin); critical revision
of the manuscript for important intellectual content (Drs Kalina, Kingsley,
and Halperin);study supervision (Drs Mittal, Farmer, and Halperin).
We are particularly indebted to the late Clarence J. Gibbs, Jr, PhD,
of the Laboratory of Central Nervous System Studies at the National Institute
of Neurological Disorders and Stroke. We would like to express our deep appreciation
to him, both for the assays performed in his laboratory and for his helpful
suggestions regarding the manuscript. We also gratefully acknowledge the guidance
of Martin Lesser, PhD, in performing the statistical analyses.
Corresponding author: John Halperin MD, Department of Neurology,
North Shore University Hospital, 300 Community Dr, Manhasset, NY 11030.
From the Departments of Neurology (Drs Mittal and Halperin), Pathology
(Dr Farmer), and Radiology (Drs Kalina and Kingsley), North Shore University
Hospital, Manhasset, NY; and New York University School of Medicine, New York.
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