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Brain Magnetic Resonance Imaging in Multiple-System Atrophy and Parkinson Disease
A Diagnostic Algorithm
Kirsty Bhattacharya, MD;
Daniela Saadia, MD;
Barbara Eisenkraft, MD;
Melvin Yahr, MD;
Warren Olanow, MD;
Burton Drayer, MD;
Horacio Kaufmann, MD
Arch Neurol. 2002;59:835-842.
ABSTRACT
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Background Brain magnetic resonance (MR) imaging offers the potential for objective
criteria in the differential diagnosis of multiple system atrophy with predominant
parkinsonism (MSA-P) and Parkinson disease (PD), since it frequently shows
characteristic abnormalities in patients with MSA-P and is believed to be
normal in patients with PD.
Objective To determine concordance between clinical and MR imaging–based
diagnoses of MSA-P and PD.
Design Two neuroradiologists identified and rated striatal and infratentorial
abnormalities in 39 brain MR images and assigned a diagnosis of PD, MSA-P,
or MSA with additional marked cerebellar ataxia (MSA-C).
Setting Academic medical center.
Patients Thirty-nine patients with parkinsonism, including 21 with a clinical
diagnosis of PD, 14 with MSA-P, and 4 with MSA-C.
Results All patients with MSA and 14 (67%) of 21 patients with PD had some abnormality
on brain MR imaging. Brainstem atrophy was seen in patients with MSA-P and
MSA-C. Putaminal atrophy was seen only in MSA-P. Putaminal hypointensity and
lateral slitlike hyperintensity were seen in both PD and MSA-P but were always
mild in PD. Cerebellar abnormalities, seen in all patients with MSA-C and
11 patients with MSA-P, were also identified in 6 patients with PD, albeit
always rated as mild. Nonconcordance between clinical and radiological diagnosis
occurred in 2 patients with PD, 5 with MSA-P, and 1 with MSA-C.
Conclusion Since several features on brain MR imaging are seen only in MSA-P, a
simple diagnostic algorithm may improve the MR imaging diagnosis of MSA-P
and PD.
INTRODUCTION
MULTIPLE-SYSTEM atrophy (MSA) and Parkinson disease (PD) are the 2 most
prevalent neurodegenerative disorders that exhibit features of parkinsonism
and autonomic dysfunction. Many patients with MSA have, in addition to parkinsonism,
cerebellar ataxia, and this combination is referred to as MSA-C. In the most frequent type of MSA, referred to as MSA-P, patients have mostly parkinsonian and few, if any, cerebellar
signs.1 Accordingly, the clinical distinction
between MSA-P and PD is often difficult. Clinical history may be helpful because,
in patients with MSA-P, symptoms of autonomic failure frequently precede parkinsonism
but, not infrequently, parkinsonism is the presenting feature. Complicating
matters further, although patients with PD usually present with parkinsonism,
they may also have severe autonomic failure in a later phase of the disease,
making the distinction from MSA-P extremely difficult. The availability of
new surgical and pharmacologic therapies that may be effective only in patients
with PD has heightened the need for precise diagnosis.
In addition to clinical criteria, several tests are proposed to distinguish
between these disorders. The most commonly used is the therapeutic response
to dopaminergic agents, the lack of which suggests a diagnosis of MSA-P. However,
pharmacologic challenge is not specific, as many patients with MSA-P may initially
respond to dopaminergic drugs. Other tests include neuroendocrine responses
to hypotension or centrally acting adrenergic agonists, which are blunted
in patients with MSA-P but preserved in patients with PD because brainstem-hypothalamic-pituitary
pathways are affected only in MSA-P.2-3
Similarly, sphincter electromyography may show denervation in patients with
MSA-P, because the Onuf nucleus, which houses preganglionic parasympathetic
neurons in segments S2 to S4 of the spinal cord, is affected in patients with
MSA-P but is normal in patients with PD.4 However,
these diagnostic tests are frequently ambiguous, their sensitivity and specificity
are controversial, and, most important, they are not widely available.
Magnetic resonance (MR) imaging of the brain is widely available and
frequently shows abnormalities in the striatum, brainstem, and cerebellum
in patients with MSA-P.5-22
Therefore, MR imaging may be a useful aid to clinical diagnosis. In this study,
neuroradiologists who were blind to the clinical diagnosis rated brain MR
images of patients with clinically diagnosed PD, MSA-P, and MSA-C. On the
basis of previously published characteristic MR imaging abnormalities,5-22
neuroradiologists assigned a diagnosis of PD, MSA-P, or MSA-C to each MR image.
The concordance between the clinical and MR imaging diagnosis was then assessed
and an algorithm was devised to improve radiological diagnosis.
PATIENTS AND METHODS
Thirty-nine patients with parkinsonism, who were followed up at the
Mount Sinai Medical Center, New York, NY, participated in this study. Eighteen
patients had a diagnosis of probable MSA according to published criteria1 (13 men and 5 women, aged 59 ± 11 years [range,
39-74 years]; disease duration, 5 ± 2 years [range, 1-10 years]; all
ages and disease durations are expressed as mean ± SD). Fourteen had
predominantly parkinsonian signs and were classified as having MSA-P (9 men
and 5 women; age, 59 ± 11 years [range, 39-71 years]; disease duration,
5 ± 3 years [range, 1-10 years]). Four had predominantly cerebellar
features and were classified as having MSA-C (all men; age, 57 ± 12
years [range, 45-74 years]; disease duration, 4 ± 2 years [range, 3-6
years]). Twenty-one patients had a diagnosis of PD (15 men and 6 women; age,
64 ± 11 years [range, 40-81 years]; disease duration, 7 ± 6
years [range, 1-20 years]) according to United Kingdom PD Brain Bank criteria.23 No patient with PD had clinical evidence of autonomic
dysfunction. Patients with PD, MSA-P, and MSA-C had a similar age. The male-female
ratio was 15:6 in PD, 9:5 in MSA-P, and 4:0 in MSA-C.
All patients underwent 1.5-T MR imaging, with a protocol that included
sagittal T1-weighted images (repetition time/echo time, 600/14 seconds; slice
thickness, 5 mm), axial intermediate and T2-weighted sequences (repetition
time/echo time, 2500/30-90 seconds; slice thickness, 5 mm), and inversion
recovery axial T1 images (repetition time/echo time/inversion time, 2500/20/800
seconds; slice thickness, 4 mm).
Two experienced neuroradiologists (B.D. and B.E.), blind to the clinical
diagnosis, visually rated the MR images for changes previously described in
brain MR images of patients with PD, MSA-P, and MSA-C.5-22
These included (1) putaminal signal hypointensity relative to the globus pallidus
on T2-weighted images, (2) linear slitlike hyperintensity in the posterolateral
margin of the putamen on T2-weighted images, (3) putaminal atrophy, (4) cerebellar
atrophy (vermis and cerebellar hemispheres), (5) brainstem atrophy (midbrain,
pons, and medulla), (6) decreased width of the substantia nigra pars compacta,
and (7) abnormal signal intensity in the middle cerebellar peduncles. Images
were rated on a scale from 0 to 3, where 0 was normal; 1, mild; 2, moderate;
and 3, severe abnormalities.
The raters gave a radiological diagnosis of PD, MSA-P, or MSA-C to each
MR image. A radiological diagnosis of MSA-P was based on findings of moderate
to severe putaminal abnormalities or mild putaminal change together with brainstem
or cerebellar abnormality. A radiological diagnosis of PD was based on near-normal
MR images, with few or no abnormalities, or the presence of only mild abnormality
in the putamen, brainstem, or cerebellum. A radiological diagnosis of MSA-C
was given if cerebellar changes in the brainstem or cerebellum were moderate
or severe regardless of putaminal change. In addition, the neuroradiologists
used their overall impression to assign a diagnosis.
Statistical analysis was performed with Fisher exact t test for qualitative MR imaging variables and t test for analysis of unpaired quantitative independent variables.
Significance was set at P = .05.
RESULTS
MR IMAGING FINDINGS
Putamen
No patient with PD had atrophy of the putamen, but 11 had slitlike hyperintensity
of its posterolateral margin and 6 had hypointensity of its body relative
to the globus pallidum, always graded as mild (grade 1) (Table 1; Figure 1) with
the exception of 1 patient, in whom slitlike hyperintensity was graded as
moderate. Patients with PD with putaminal rim hyperintensity were significantly
older than those without this finding (68 ± 10 vs 59 ± 10 years; P = .02). Six patients with MSA-P had atrophy of the putamen
(P = .002 vs PD); 11 had slitlike hyperintensity
of its posterolateral margin (P = .16 vs PD), graded
as mild in 6 and moderate or severe in 5 (P = .006
vs PD); and 11 had hypointensity of its body (P =
.006 vs PD), graded as mild in 5 and moderate or severe in 6 (P = .002 vs PD) (Figure 2).
Contrary to patients with PD, patients with MSA-P with and without putaminal
rim hyperintensity were of a similar age. No patient with MSA-C had atrophy
of the putamen, but 3 had mild hypointensity of its body and 2 had mild slitlike
hyperintensity of its posterolateral margin.
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Table 1. Brain MR Imaging Findings in Patients Clinically Diagnosed
With MSA-P, PD, and MSA-C*
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Figure 1. A, Normal iron distribution, ie,
globus pallidum hypointensity relative to the putamen in a patient with a
clinical diagnosis of Parkinson disease (axial section, 1.5 T, T2 weighting).
B, Reversal of normal iron distribution with severe putaminal hypointensity
relative to the globus pallidum (inset) in a patient with a clinical diagnosis
of multiple-system atrophy with predominant parkinsonism (axial section, 1.5
T, T2 weighting). C, Normal iron distribution in the globus pallidum relative
to the putamen in a patient with a clinical diagnosis of Parkinson disease
(coronal section, 1.5 T, T2 weighting). D, Reversal of normal iron distribution
with mild putaminal hypointensity relative to the globus pallidum (arrow)
in a patient with a clinical diagnosis of multiple-system atrophy with predominant
parkinsonism (coronal section, 1.5 T, T2 weighting).
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Figure 2. A, Normal posterolateral putaminal
margin in a patient with a clinical diagnosis of Parkinson disease (axial
section, 1.5 T, T2 weighting). B, Mild slitlike hyperintensity of the posterolateral
putaminal rim (inset, arrow) in a patient with a clinical diagnosis of multiple-system
atrophy with predominant parkinsonism (axial section, 1.5 T, T2 weighting).
C, Moderate slitlike hyperintensity of the posterolateral putaminal rim (inset,
arrow) in a patient with a clinical diagnosis of multiple-system atrophy with
predominant parkinsonism (axial section, 1.5 T, T2 weighting).
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Substantia Nigra
Decreased width of the substantia nigra pars compacta was identified
in 1 of 21 patients with PD and "smudging" of its posterior border in 2. No
patient with either MSA-P or MSA-C had radiological changes in the substantia
nigra.
Brainstem Findings
No patient with PD had brainstem atrophy. Seven patients with MSA-P
had brainstem atrophy (Figure 3).
Five patients had atrophy affecting the midbrain (rated mild in 4 and moderate
in 1), 6 patients had atrophy affecting the pons (rated mild in 5 and moderate
in 1), and 6 patients had atrophy affecting the medulla (rated mild in 4 and
moderate in 2). Cruciform hyperintensity of the pons, the "hot-cross bun"
sign (Figure 4), was present in
1 patient.
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Figure 3. A, Normal brainstem and cerebellum
in a patient with a clinical diagnosis of Parkinson disease (sagittal section,
1.5 T, T1 weighting). B, Mild brainstem and cerebellar atrophy in a patient
with a clinical diagnosis of multiple-system atrophy with predominant parkinsonism
(sagittal section, 1.5 T, T1 weighting). C, Severe brainstem and cerebellar
atrophy in a patient with a clinical diagnosis of multiple-system atrophy
with predominant parkinsonism (sagittal section, 1.5 T, T1 weighting).
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Figure 4. A, Normal pons in a patient with
a clinical diagnosis of Parkinson disease (axial section, 1.5 T, T2 weighting).
B, "Hot-cross bun" sign: cruciform degeneration of pontine fibers secondary
to brainstem atrophy (inset) in a patient with a clinical diagnosis of multiple-system
atrophy with predominant parkinsonism (axial section, 1.5 T, T2 weighting).
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Brainstem atrophy was seen in 3 patients with MSA-C. Two patients had
moderate atrophy in all brainstem areas. The hot-cross bun sign was present
in 2.
Cerebellar Findings
Six patients with PD had some cerebellar abnormality, all rated mild.
All 6 of these patients had atrophy of the vermis and 3 had atrophy of the
cerebellar hemispheres. One patient had mild signal abnormality in the middle
cerebellar peduncle (Figure 5). Eleven patients with MSA-P had cerebellar abnormalities (P = .006 vs PD), 7 had atrophy of the cerebellar vermis, 5 mild and
2 moderate; 6 had atrophy of the cerebellar hemispheres, 5 mild and 1 moderate;
and 3 had abnormal signal in the middle cerebellar peduncle, 1 mild, 1 moderate,
and 1 severe.
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Figure 5. A, Normal cerebellum in a patient
with a clinical diagnosis of Parkinson disease (axial section, 1.5 T, T2 weighting).
B, Abnormal signal in the middle cerebellar peduncles (arrow) in a patient
with a clinical diagnosis of multiple-system atrophy with predominant parkinsonism
(axial section, 1.5 T, T2 weighting).
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All patients with MSA-C had cerebellar abnormalities; all had atrophy
of the vermis, 1 mild, 2 moderate, and 2 severe; 3 had atrophy of the cerebellar
hemispheres, 1 mild, 1 moderate, and 1 severe; and 2 had abnormal signal in
the middle cerebellar peduncles, 1 mild and 1 moderate. The combination of
infratentorial and putaminal abnormalities was present in 6 patients with
PD, 10 with MSA-P (P = .02 vs PD), and all patients
with MSA-C.
CONCORDANCE BETWEEN RADIOLOGICAL AND CLINICAL DIAGNOSIS
The neuroradiologists "erroneously" diagnosed 5 patients with a clinical
diagnosis of MSA-P as having PD (Table 2). Of these, mild atrophy of the putamen was present in 1, 3 had
mild hypointensity of its body, and 4 had mild hyperintensity of its posterolateral
margin. Two of these patients had brainstem atrophy and 2 had mild cerebellar
atrophy. Patients with MSA-P "wrongly" diagnosed radiologically as having
PD had significantly shorter disease duration (4 ± 1 vs 6 ±
3 years; P = .05), although they were of similar
age in comparison with patients with MSA-P "correctly" diagnosed by the neuroradiologists.
The neuroradiologists "erroneously" diagnosed 2 patients with a clinical diagnosis
of PD as having MSA-P. One patient had mild signal abnormality in the middle
cerebellar peduncle and the other had mild putaminal and cerebellar abnormalities.
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Table 2. Brain MR Imaging Findings in Patients With MSA-P With Concordant
Radiological Diagnosis of MSA-P and Nonconcordant Radiological Diagnosis of
PD*
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The 1 patient with MSA-C "erroneously" diagnosed by the neuroradiologists
as having PD had only mild changes in the putamen, brainstem, and cerebellum.
COMMENT
We found that several features on brain MR images of patients with parkinsonism
are diagnostic of MSA-P, as they are never seen in patients with PD. These
included putaminal and brainstem atrophy and abnormal signal in the middle
cerebellar peduncles. Other abnormalities were found in both patients with
MSA-P and those with PD, but they varied in severity. These included hypointensity
of the putaminal body, slitlike hyperintensity of the lateral putaminal border,
and atrophy of the cerebellar vermis or hemispheres. When the severity of
these abnormalities was graded, it was always mild in patients with PD. All
patients with MSA-P and two thirds of patients with PD had some abnormality
on brain MR imaging.
Two patients with PD were assigned a diagnosis of MSA-P by the neuroradiologists.
One was a 38-year-old woman with onset of PD at age 18 years. On MR imaging
she had mild signal change in the middle cerebellar peduncle. We speculate
that patients with juvenile-onset PD may have different MR imaging characteristics
than those in patients with adult-onset PD. The other patient was a 68-year-old
man with disease duration of 4 years, asymmetric onset of tremor, excellent
levodopa responsiveness, and dyskinesias, making a diagnosis of MSA-P unlikely.
On brain MR imaging, he had mild hypointensity of the body of the putamen,
mild hyperintensity of its lateral rim, and mild atrophy of the cerebellar
vermis and hemispheres.
The 5 patients with MSA-P, assigned an MR imaging diagnosis of PD by
the neuroradiologists, had, in general, mild putaminal and cerebellar abnormalities
on brain MR images. Their mean disease duration was less than 5 years (range,
1-5 years), significantly shorter than that of patients with MSA-P assigned
the "correct" MR imaging diagnosis. Brain MR imaging may be of limited value
in patients with MSA-P early in their disease, as it may show only mild abnormalities.
However, in these 5 patients there were abnormalities present, which were
specific to MSA-P; 1 patient had mild atrophy of the putamen and 2 had brainstem
atrophy. The patient with MSA-C neuroradiologically diagnosed as having PD
had only mild putaminal and cerebellar abnormalities but also mild brainstem
atrophy, an abnormality not found in patients with PD. In sum, nonconcordance
between clinical and radiological diagnoses occurred in cases with mild putaminal
hypointensity, mild hyperintensity of the lateral putaminal border, and mild
cerebellar atrophy, which were abnormalities found in all 3 patient groups.
Identifying abnormalities found only in MSA-P, such as atrophy of the putamen
and brainstem or abnormal signal change in the cerebellar peduncle, improves
the accuracy of radiological diagnosis in MSA-P and PD.
We therefore propose a simple diagnostic algorithm for the diagnosis
of PD and MSA-P using brain MR images (Figure
6). Atrophy of the putamen or brainstem and abnormal signal in the
middle cerebellar peduncle are diagnostic of MSA-P. Hypointensity of the body
of the putamen, hyperintensity of its lateral rim, and atrophy of the cerebellar
vermis and hemispheres are found in both MSA-P and PD and are diagnostic of
MSA-P only when severity is rated as more than mild, ie, moderate or severe.
Mild putaminal hypointensity, mild putaminal lateral slitlike hyperintensity,
and mild cerebellar atrophy could represent PD or early MSA-P of less than
5 years' duration, and thus follow-up MR imaging is needed. If brain MR imaging
is normal, the patient could have PD or MSA-P of less than 1 year's duration,
as, although MR imaging was abnormal in all patients with MSA-P, no patient
had disease duration of less than 1 year.
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Figure 6. Algorithm for the magnetic resonance
(MR) imaging diagnosis of multiple-system atrophy with predominant parkinsonism
(MSA-P) and Parkinson disease (PD). Red indicates MR imaging diagnosis of
MSA-P; blue, MR imaging diagnosis of PD; green, MR imaging diagnosis of PD
or early MSA-P; and MCP, middle cerebellar peduncles.
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With this algorithm, the 3 patients with MSA-P and the 1 patient with
MSA-C "wrongly" diagnosed radiologically as having PD would not have been
assigned a brain MR imaging diagnosis of MSA-P or MSA-C, as they had abnormalities
never found in patients with PD. Therefore, the proposed algorithm increases
the concordance between radiological and clinical diagnoses.
The major limitation of this algorithm is that it has not been validated
by neuropathologic data and clinical diagnosis could be wrong. It is possible
that patients with PD who had MR imaging abnormalities could have received
an incorrect clinical diagnosis and actually had MSA-P, and that patients
with MSA-P who had mild MR imaging abnormalities could have indeed had PD.
However, several factors suggest that the clinical diagnosis was the right
one. First, during an average of 7 years of follow-up, no patient with clinically
diagnosed PD developed signs or symptoms suggestive of MSA-P,24
but this is not conclusive. Second, all patients with clinically diagnosed
PD had asymmetric onset of symptoms and signs and were levodopa responsive,
and almost all developed dyskinesias over time, features unusual in MSA-P
but again nonconclusive. Similarly, several factors suggest that the clinical
diagnosis was the correct one in MSA-P. All patients with MSA-P had early
autonomic failure, had symmetric onset of parkinsonism, were poorly levodopa
responsive or were levodopa unresponsive, and, within an average of 5 years
of follow-up, did not develop dyskinesias.
Atrophy of the putamen and moderate or severe hypointensity of its body
were found only in patients with MSA-P and not in patients with PD or MSA-C.
This suggests that putaminal atrophy and hypointensity of the putaminal body,
thought to be due to increase in iron deposition in the putamen,5-6
are indicative of "end-organ" striatal damage, as they were not present or
were mild in patients with PD or MSA-C with mild extrapyramidal signs but
were present with increased severity in patients with MSA-P and severe extrapyramidal
signs. This is in agreement with previous studies finding correlation between
degree of putaminal atrophy and severity of extrapyramidal signs.17, 21-22
Slitlike hyperintensity of the posterolateral putaminal margin has not,
to our knowledge, been reported in PD.18 We
found definite but mild slitlike hyperintensity of the lateral putamen in
11 of 21 patients with a clinical diagnosis of PD. Mild putaminal rim hyperintensity
is frequently seen on brain MR images in normal aging (B.D., unpublished data,
2000) and may represent age-related reactive gliosis. Interestingly, patients
with PD who have this finding were significantly older than those without
it. We found that all patients with MSA-P with pronounced putaminal rim hyperintensity
had concomitant putaminal atrophy, suggesting that marked putaminal rim hyperintensity
may be due to extracellular fluid accumulation in the putaminal capsule secondary
to atrophy of the nucleus.20
Although radiological abnormalities of the substantia nigra, including
decreased width and smudging of its posterior border, have been reported in
MSA-P, MSA-C, and PD, we found a low frequency, in only 2 of 21 patients with
PD and no patients with MSA-P or MSA-C. Therefore, substantia nigra abnormality
was not included in the algorithm.
In conclusion, it is often difficult to distinguish clinically between
patients with MSA-P and PD, and high–field-strength brain MR images
may be useful, as patients with MSA-P show specific abnormalities that can
distinguish them from patients with PD. Other abnormalities are found in both
disorders, but, when the severity of the abnormality is graded, it is always
mild in patients with PD. On the basis of these findings, we have designed
a simple algorithm to help distinguish patients with MSA-P from patients with
PD by means of brain MR imaging.
AUTHOR INFORMATION
Accepted for publication January 22, 2002.
Author contributions: Study concept and design (Drs Bhattacharya, Saadia, Yahr, Drayer, and Kaufmann); acquisition
of data (Drs Bhattacharya, Saadia, Eisenkraft, Olanow, Drayer,
and Kaufmann); analysis and interpretation of data (Drs Bhattacharya, Saadia, Eisenkraft, Drayer, and Kaufmann); drafting
of the manuscript (Drs Bhattacharya, Saadia, Drayer, and
Kaufmann); critical revision of the manuscript for important intellectual
content (Drs Bhattacharya, Saadia, Eisenkraft, Yahr, Olanow,
Drayer, and Kaufmann); statistical expertise (Drs
Bhattacharya, Saadia, and Kaufmann); administrative, technical, or
material support (Drs Eisenkraft and Drayer); study
supervision (Drs Yahr, Olanow, Drayer, and Kaufmann).
Corresponding author and reprints: Horacio Kaufmann, MD, Mount Sinai
School of Medicine, Campus Box 1052, New York, NY 10029 (e-mail: Horacio.Kaufmann{at}mssm.edu).
From the Departments of Neurology (Drs Bhattacharya, Saadia, Yahr,
Olanow, and Kaufmann) and Radiology (Drs Eisenkraft and Drayer), Mount Sinai
School of Medicine, New York, NY.
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MR Imaging Index for Differentiation of Progressive Supranuclear Palsy from Parkinson Disease and the Parkinson Variant of Multiple System Atrophy
Quattrone et al.
Radiology 2007;246:214-221.
ABSTRACT
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Usefulness of combined fractional anisotropy and apparent diffusion coefficient values for detection of involvement in multiple system atrophy
Ito et al.
J. Neurol. Neurosurg. Psychiatry 2007;78:722-728.
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Apparent diffusion coefficient measurements of the middle cerebellar peduncle differentiate the Parkinson variant of MSA from Parkinson's disease and progressive supranuclear palsy
Nicoletti et al.
Brain 2006;129:2679-2687.
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Is it Parkinson's disease, and if not, what is it?
Taylor and Counsell
PN 2006;6:154-165.
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MR Imaging of Middle Cerebellar Peduncle Width: Differentiation of Multiple System Atrophy from Parkinson Disease.
Nicoletti et al.
Radiology 2006;239:825-830.
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Hyperintense Putaminal Rim Sign Is Not a Hallmark of Multiple System Atrophy at 3T
Lee et al.
Am. J. Neuroradiol. 2005;26:2238-2242.
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Management of Hypertension in the Setting of Autonomic Failure: A Pathophysiological Approach
Shibao et al.
Hypertension 2005;45:469-476.
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Field strengths and sequences influence putaminal MRI findings in multiple system atrophy
Watanabe et al.
Neurology 2004;62:671-671.
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Fragile X Premutation Carriers: Characteristic MR Imaging Findings of Adult Male Patients with Progressive Cerebellar and Cognitive Dysfunction
Brunberg et al.
Am. J. Neuroradiol. 2002;23:1757-1766.
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