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Crossed Cerebellar Atrophy in Patients With Precocious Destructive Brain Insults
Ricardo A. Teixeira, MD;
Li M. Li, MD, PhD;
Sergio L. M. Santos, MD;
Veronica A. Zanardi, MD, PhD;
Carlos A. M. Guerreiro, MD, PhD;
Fernando Cendes, MD, PhD
Arch Neurol. 2002;59:843-847.
ABSTRACT
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Objective To analyze the frequency and pathogenetic factors of crossed cerebellar
atrophy (CCA) in adult patients with epilepsy secondary to destructive brain
insults of early development.
Methods We studied 51 adult patients with epilepsy and precocious destructive
lesions. Patients were divided into 3 groups according to the topographic
distribution of their lesions on magnetic resonance imaging: group A, hemispheric
(n = 9); group B, main arterial territory (n = 25); and group C, arterial
border zone (n = 17). We evaluated the presence of CCA visually and with cerebellar
volumetric measurement, correlating it with the clinical data. Other features
shown on magnetic resonance imaging, such as the thalamus, brainstem, and
middle cerebellar peduncle, were also carefully analyzed.
Results Seven patients (13%) had CCA that was associated with the extent of
the supratentorial lesion (6 from group A, 1 from group B, and none from group
C; P<.001). Status epilepticus was present in
6 patients from group A and in none from the other groups. There was an association
between the antecedent of status epilepticus and CCA (P<.001). All patients had atrophy of the cerebral peduncle ipsilateral
to the supratentorial lesion and 4 had contralateral atrophy of the middle
cerebellar peduncle. The duration of epilepsy was not associated with the
presence of CCA (P = .20).
Conclusions Our data suggest that in patients with epilepsy and destructive insults
early in life, the extent of the supratentorial lesion as well as the antecedent
of status epilepticus play a major role in the pathogenesis of CCA. Recurrent
seizures do not seem to be relevant to the development of CCA.
INTRODUCTION
ATROPHY OF the cerebellum contralateral to a hemispheric supratentorial
lesion, or crossed cerebellar atrophy (CCA), has been recognized by neuropathologists
for more than 100 years but the understanding of its pathogenesis is still
incomplete.1-7
In 1980, Baron et al8 described contralateral
cerebellar hypometabolism (CCH) in positron emission tomographic (PET) images
of adult patients with supratentorial infarcts, calling it crossed cerebellar diaschisis. Diaschisis is also an old concept, classically
defined as a transient impairment of functional activity in an area remote
from the site of a primary lesion.9-10
However, the interpretation of CCH as a diaschisis is challenged since there
are several instances in which the CCH lacks reversibility.11-12
Thus, a reversible diaschisis and an irreversible atrophy can hypothetically
constitute the extremes of a continuum of the same biological process. Damage
to the corticopontocerebellar pathway is the most accepted pathogenic mechanism
in the development of CCH or CCA.13-15
There is also a robust body of evidence on the destructive effects of prolonged
seizures in vulnerable regions of the brain and on the damage caused by partial
status epilepticus (SE) to the contralateral cerebellum.16-20
The role of the extension of the cerebral lesion in CCH is not fully
understood since it has been associated with the degree of CCH in some studies11, 21 but not in others.22-23
Furthermore, the role of recurrent seizures in the development of CCH or CCA
is not yet clear.5, 8, 24
To further investigate the pathogenesis of CCA, we reviewed the results of
magnetic resonance imaging (MRI) in a series of patients with epilepsy and
different types of destructive lesions of early development to assess whether
there is any particular MRI or clinical feature related to CCA.
METHODS
We evaluated the MRI results of 51 consecutive adult patients with the
diagnosis of epilepsy secondary to a destructive brain lesion of early development,
who were seen at our institution from March 1999 to April 2001 (median age,
31.8 years; range, 15-55 years). Detailed histories of prenatal, neonatal,
and early childhood events were systematically reviewed in the medical records,
and direct interviews with the patients and their relatives were conducted.
All patients had disease onset before the age of 5 years; we excluded all
patients with evidence of adult-onset disease. Informed consent was obtained
from all subjects. This study was approved by the ethics committee of the
faculty of medical sciences of University of Campinas (Campinas, Brazil).
Magnetic resonance imaging was performed by a 2.0 T scanner (Elscint
Prestige, Haifa, Israel). Our epilepsy protocol consists of: (1) sagittal
T1 spin-echo, 6 mm thick (repetition time [TR], 430; echo time [TR], 12) for
optimal orientation of the subsequent images; (2) coronal T1 inversion recovery,
3 mm thick (tip angle, 200°; TR, 2700; TE, 14; TI, 840; matrix, 130 x
256; field of view [FOV], 16 x 18 cm); (3) coronal T2-weighted fast
spin-echo, 3 to 4 mm thick (tip angle, 120°; TR, 4800; TE, 129; matrix,
252 x 320; FOV, 18 x 18 cm); (4) axial images parallel to the
long axis of the hippocampus; T1 gradient echo, 3 mm thick (tip angle, 70°;
TR, 200; TE, 5; matrix, 180 x 232; FOV, 22 x 22 cm); (5) axial
T2 fast spin-echo, 4 mm thick (tip angle, 120°; TR, 6800; TE, 129; matrix,
252 x 328; FOV, 21 x 23 cm); and (6) volumetric (3-dimensional)
T1 gradient echo, acquired in the sagittal plane for multiplanar reconstruction,
1 to 1.5 mm thick (tip angle, 35°; TR, 22; TE, 9; matrix, 256 x
220; FOV, 23 x 25 cm).
Visual analysis of MRI results was systematically performed by one of
us (S.L.M.S.), blinded to the clinical data, in a workstation (Silicon Graphics
O2; Silicon Graphics Computer Systems, Mountain View, Calif) using
Omnipro software (Elscint Prestige). Curvilinear reconstruction of 3-dimensional
MRI volumetric images was performed in all patients by a Power MacIntosh (Apple
Computer Inc, Cupertino, Calif) using the Brainsight software (Rogue Research,
Montreal, Quebec). This approach was very helpful for clear visualization
of the extent of cortical involvement and allowed us to classify the patients
into 3 different groups according to the topographical distribution of the
lesion: group A, hemispheric lesions, defined as a diffuse atrophy of an entire
hemisphere without loss of tissue continuity (n = 9); group B, lesions limited
to a main arterial territory, often constituting a cavity (n = 25); and group
C, lesions on the border zones between the main cerebral arterial territories
(n = 17)25-26 (Figure 1). Special attention was also focussed on the morphology
of the brainstem, thalamus, cerebellum, and middle cerebellar peduncle.
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Figure 1. Curvilinear reconstruction of
3-dimensional acquisitions and axial images from different patients illustrating
the 3 groups. A, Diffuse atrophy of the right cerebral hemisphere. B, Large
cavity on the territory of the right middle cerebral artery (MCA). C, Bilateral
atrophy on the border zone between the 3 main arterial territories, with a
left predominance (black arrows) also shown on the axial image. Discrete left
parasagittal atrophy can be observed on the border zone between the anterior
cerebral artery and the MCA (white arrow).
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In addition, we performed volumetric measurements of the cerebellums
of all patients using a semiautomatic software program (NIH-Image; National
Institute of Health, Bethesda, Md). The cerebellum was manually outlined on
sagittal slices. To check right-left asymmetry, the measurements were distributed
into right and left cerebellum according to the position of the cerebral aqueduct.
When only 1 slice showed the cerebral aqueduct, half of its measurement was
computed to the right cerebellum and the other half to the left. More commonly,
2 slices showed the cerebral aqueduct, and in these cases, each slice was
computed to each hemicerebellum. The extracerebellar portion of the middle
cerebellar peduncle was not included and this limit was assumed as the angle
formed between the cerebellar hemisphere and the middle cerebellar peduncle.
The cerebellums of 12 healthy volunteers were measured and constituted
a control group. An asymmetry index (AI) was calculated for each subject by
subtracting the right hemicerebellum volume from the left and then dividing
by the mean of the right and left. Values outside 2 SDs (95% confidence interval)
from the AI mean of the control group were considered abnormal. Cerebellar
volume was normalized to the total brain volume to check for bilateral atrophy.
We used the Pearson  2 test and Fisher exact test for
comparisons between proportions. An analysis of variance and the Tukey post
hoc pairwise comparison were applied for comparison on continuous variables
among the 3 groups. We used the Pearson correlation test to assess correlation
between duration of epilepsy and cerebellar volumes. The significance level
was .05.
RESULTS
Crossed cerebellar atrophy was visually identified in 6 patients. The
volumetric studies confirmed the CCA in these 6 patients and in a seventh
patient whose visual analysis did not definitively point to CCA. A visual
diagnosis of bilateral cerebellar atrophy was made in 9 patients, all of whom
had long-term exposure to phenytoin. These patients showed thinner folia but
had preservation of the cerebellar contour dimension so that while results
of their volumetric studies tended to be abnormal, they did not reach significance.
None of the patients with cerebellar atrophy had clinical cerebellar signs.
Six of the 7 patients with CCA belonged to group A (hemispheric) and
1 to group B (arterial territory) (Figure
2). All 6 patients from group A had the antecedent of SE in the
first 5 years of life, developing a permanent hemiparesis just after the SE.
In 4 patients, SE associated with a febrile illness was the first manifestation
of their disease. Two patients had SE after experiencing uncomplicated seizures,
1 of them since the neonatal period. The single patient from group B did not
experience any episodes of SE and had the first seizure at age 27 years. This
patient had a right hemiparesis observed in the first year of life without
any potentially associated morbid event and had a large cystic infarct in
the territory of the left middle cerebral artery, pointing to a prenatal insult.
Patients with CCA exhibited the SE antecedent more commonly (6/7) than those
without CCA (2/44) (2 = 22.49; P<.001).
The SE antecedent was by far more common in patients in group A (8/9) than
in the other groups (group B, 1/25; group C, 1/17) (2 = 30.39; P<.001).
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Figure 2. A, A 40-year-old man who had the
antecedent of status epilepticus, which led to a left motor deficit. Coronal
inversion recovery (IR) T1-weighted image shows right hemiatrophy with left
cerebellar atrophy. B, A 51-year-old woman with a congenital right hemiparesis
and epilepsy. Coronal IR T1-weighted image demonstrates a large cavity in
the territory of the left middle cerebral artery and right cerebellar atrophy.
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The duration of epilepsy and seizure frequency were similar between
the groups and were not different in patients with CCA (P>.05). Recurrent generalized convulsions throughout the course of
epilepsy were more frequent among patients in group B (7/25) than groups A
(0/9) and C (1/17) but the difference was not statistically significant (P>.05). The frequency of generalized convulsions was also
not different between patients with CCA and those without (P>.05). Three patients from group A (33.3%), 6 patients from group
B (24%), and none from group C exhibited hemiconvulsions as a habitual seizure
type (P>.05). Hemiconvulsions were equally frequent
among patients with CCA and those without CCA (P>.05).
Ictal semiology exclusively of the temporal lobe was observed in 17 patients
(33%) and it was more common among patients in group C (2
= 11.41; P = .003).
Analysis of variance demonstrated that the AI was different among the
groups (F2,48= 7.63; P = .001) and post
hoc comparison showed that group A (mean, 3.83) was significantly different
from groups B (0.99) and C (0.82). Furthermore, no correlation was found between
duration of epilepsy and AI (R2 = 1.11; P = .3).
Four of the 7 patients with CCA exhibited atrophy of the middle cerebellar
peduncle contralateral to the supratentorial lesion. The other 3 patients
with CCA without atrophy of the cerebellar peduncle all exhibited the antecedent
of SE. In contrast, patients without CCA did not exhibit atrophy of the middle
cerebellar peduncle.
Atrophy of the ipsilateral cerebral peduncle was more commonly observed
in patients from groups A (8/9) and B (18/25) than from group C (4/13) (2 = 13.89; P = .001). All patients with CCA
had ipsilateral cerebral peduncle atrophy and 2 of them also exhibited atrophy
of the ipsilateral pons (Figure 3).
Ipsilateral thalamus involvement was more frequent in patients from groups
A and B (5/9 and 17/25, respectively) than in group C (2/15) (2 = 13.16; P = .001). There was atrophy of the
ipsilateral thalamus in all patients with CCA except one. Both thalamus and
brainstem involvement were associated with the presence of CCA (Fisher exact
test, P<.005).
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Figure 3. A 42-year-old woman with mental
retardation and epilepsy, who had febrile status epilepticus followed by left
hemiparesis at the age of 11 months. A, Coronal inversion recovery T1-weighted
image shows right hemiatrophy and marked contralateral cerebellar atrophy.
B, Axial T1-weighted image shows atrophy of the cerebral peduncle ipsilateral
to the supratentorial lesion (arrow). C, Axial T1-weighted image exhibits
atrophy of the middle cerebellar peduncle contralateral to the supratentorial
lesion (arrow).
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COMMENT
In their classic article, Verhaart and Van Wieringen-Rauws2
observed that CCA tends to be associated with long-standing, extensive unilateral
lesions of the cerebral hemisphere, usually originating in infancy or early
childhood. Thirty years later, Baron et al8
described CCH observed on PET scans of adult patients with supratentorial
infarcts, suggesting that it represents the "early metabolic correlate of
the phenomenon of CCA." Since then, it has been well accepted that CCH and
CCA constitute a spectrum of the same biological process but the factors that
determine a reversible and functional phenomenon (CCH) to become an irreversible
structural change (CCA) are still not fully understood.
Tien and Ashdown12 were the first to
report the possible connections between CCH and CCA, analyzing the MRIs of
patients with CCH observed on PET scan images. They found that 8 of 26 patients
with CCH also had CCA. All 8 patients had long-standing unilateral hemispheric
atrophy with intractable focal seizures. Conversely, most patients without
CCA had cerebral tumors larger than 3 cm, and only 40% had seizures. Those
patients were older and had shorter duration of symptoms than the patients
with CCA. This study suggests that the differentiation of CCH from CCA depends
on the nature and extension of the lesion and the duration of symptoms, as
well as on the age of the patient at illness onset. Cautiously, the authors
suggest that recurrent seizures can also play a role in CCA but unfortunately
no mention was made of the SE antecedent in these patients.
In our study, all patients who had CCA had extensive unilateral hemispheric
lesions. Most of the patients from group C (arterial border zone) had bilateral
and small lesions, and none of them exhibited CCA. Of particular interest
is the finding that CCA was almost exclusively present among patients with
hemiatrophy (group A). Only 1 patient in group B (arterial territory) had
CCA, although most of the patients in this group also had long-standing and
extensive unilateral lesions with ipsilateral atrophy of the brainstem. Some
other factor in addition to the extension of the lesion must have played a
key role in the development of CCA in these patients. Status epilepticus seems
to have been a contributing factor, considering that it was much more frequent
in group A than in the other groups. Since sequential MRI studies before and
after SE are not available, it could be argued that SE is associated more
with the extent of cerebral injury rather than specifically with CCA. However,
there is major evidence that primary damage to a hemicerebellum is caused
by a lateralized SE.14-15,20
Strefling and Urich15 emphasized that
severe epileptic seizures are probably one of the most important causes of
CCA and proposed 2 main distinct patterns of CCA, one of them associated with
transneuronal degeneration and the other with postictal damage. Tan and Urich15 described the necropsy findings of a patient who
died 2 days after a lateralized SE and compared them with findings from 3
necropsies of patients who had exhibited the antecedent of SE months or years
before death. There was no difference in the extent or distribution of neuronal
necrosis between the acute and chronic cases, suggesting that SE was sufficient
to cause the pattern of lesions observed in the chronic cases. All cases had
unilateral hemispheric necrosis with damage of the contralateral cerebellum.15
Men et al20 described a patient who experienced
2 generalized uncomplicated seizures and was found to have a small temporal
lobe lesion on MRI that was suggestive of a tumor. The patient died 6 days
after a lateralized SE with predominant motor manifestations on the right
hemibody that culminated in multiorgan failure. The neuropathologic findings
included laminar cortical necrosis in the left hemisphere associated with
a marked loss of Purkinje cells in the right hemicerebellum. The presence
of eosinophilic changes on many of the remaining Purkinje cells of the affected
hemicerebellum pointed to recent damage. In addition, MR diffusion-weighted
images (2 days before death) showed abnormal diffusion throughout the cortex
of the left hemisphere and right hemicerebellum.
Other authors have suggested that repetitive seizures could be a main
pathogenetic factor in CCA.5, 8, 24
Our study does not support this concept since the duration of epilepsy and
seizure frequency was similar between the groups and it was not different
among the patients with CCA. In addition, the pattern of seizure semiology
did not seem to have an effect on CCA in our series. Neither hemiconvulsions
nor generalized convulsions recurring long after the onset of epilepsy were
different among the groups or between patients with CCA and those without.
Patients with arterial border zone lesions more commonly exhibited monomorphic
seizure semiology with a temporal lobe–like pattern (probably reflecting
their less extensive lesions), and we cannot discard the possibility that
this might be associated with the absence of CCA in this group of patients.
However, it seems unlikely that seizure semiology had a greater influence
on CCA compared with the extension and bilaterality of the lesion in these
patients. Given the few patients with CCA, it is likely that the power of
this study is insufficient to conclude that there is a definite negative relationship
between habitual seizures and CCA.
There is evidence that transneuronal degeneration has a decisive role
in the pathogenesis of CCA. Necropsy studies of patients with CCA commonly
show atrophy of the middle cerebellar peduncle contralateral to the supratentorial
lesion and in the nuclei of the ipsilateral pons.14-15
A more recent work, using PET studies of patients with supratentorial tumors,
showed a significant reduction in glucose metabolism in the ipsilateral pons
parallel to CCH.13 Patients with long-standing
supratentorial damage but no history of seizures can occasionally develop
CCA.27-28 Moreover, there is a
report that describes a patient who developed CCA after a hemispherectomy
for seizure control.29
Cerebral peduncle atrophy ipsilateral to the supratentorial lesion was
significantly associated with CCA in our study. This can be interpreted as
a sign of wallerian degeneration but can also represent the primary lesion.
Conversely, the contralateral middle cerebellar peduncle atrophy observed
in 4 of the patients with CCA should be considered as a sign of transneuronal
degeneration associated with damage to the corticopontinecerebellar pathway.15 One of these patients did not have the SE antecedent;
the transneuronal degeneration seemed to be the main mechanism of CCA in this
case. In contrast, there were 3 patients without atrophy of the middle cerebellar
peduncle but who had a history of SE. In these cases, SE may have been the
cause of CCA, even without late transneuronal degeneration.
Another possible factor involved in the pathogenesis of CCA is the damage
to the cerebellorubrothalamic tract leading to a retrograde CCA.30
Atrophy of the thalamus was significantly associated with the presence of
CCA in our series. However, it may have been just the reflex of the extension
of the lesion since it was also more frequent among patients in groups A and
B, who had larger lesions. Therefore, it is not possible to determine the
relative importance of retrograde CCA in these patients.
In conclusion, our study suggests that in patients with long-standing
destructive brain lesions and epilepsy, SE as well as the extent of the supratentorial
primary lesion play major roles in the development of CCA. Our data also suggest
that recurrent seizures are not relevant to the development of CCA.
AUTHOR INFORMATION
Accepted for publication December 6, 2001.
Author contributions: Study concept and design (Drs Teixeira, Li, and Cendes); acquisition of data (Drs Teixeira, Li, and Cendes); analysis and interpretation
of data (Drs Teixeira, Li, Santos, Zanardi, Guerreiro, and
Cendes); drafting of the manuscript (Drs Teixeira,
Li, and Cendes); critical revision of the manuscript for important
intellectual content (Drs Teixeira, Li, Santos, Zanardi,
Guerreiro, and Cendes); statistical expertise (Drs
Teixeira, Li, and Cendes); study supervision (Drs
Li, Santos, Zanardi, Guerreiro, and Cendes).
Dr Teixeira was supported by scholarship grant 98/13101-8 from FAPESP
(Fundação de Amparo à Pesquisa do Estado de São
Paulo, Brazil). The study was supported by grant 97/07584-3 from FAPESP (Dr
Cendes).
Corresponding author and reprints: Fernando Cendes, MD, PhD, Department
of Neurology, FCM-UNICAMP, Campinas, SP, Brazil, CEP 13083-970 (e-mail: fcendes{at}unicamp.br).
From the Departments of Neurology (Drs Teixeira, Li, Guerreiro, and
Cendes) and Radiology (Drs Santos and Zanardi), University of Campinas, Campinas,
Brazil.
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