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Figure.
 Axial T2-weighted magnetic resonance image showing severe atrophy and hyperintensities of the middle cerebellar peduncles and pons.

Axial T2-weighted magnetic resonance image showing severe atrophy and hyperintensities of the middle cerebellar peduncles and pons.

Table 1.  
 Clinical Characteristics of the 41 Study Patients
Clinical Characteristics of the 41 Study Patients
Table 2.  
 Qualitative Abnormalities on T2-Weighted Magnetic Resonance Images
Qualitative Abnormalities on T2-Weighted Magnetic Resonance Images
Table 3.  
 Correlation Analysis of Disability Scores and Semiquantitative MRI Features
Correlation Analysis of Disability Scores and Semiquantitative MRI Features
Table 4.  
 Correlation Analysis of Basal Ganglia Symptoms and Qualitative Magnetic Resonance Imaging Features
Correlation Analysis of Basal Ganglia Symptoms and Qualitative Magnetic Resonance Imaging Features
1.
Gilman  SQuinn  NP The relationship of multiple system atrophy to sporadic olivopontocerebellar atrophy and other forms of idiopathic late onset cerebellar atrophy. Neurology 1996;461197- 1199
PubMedArticle
2.
Gilman  SLow  PAQuinn  N  et al.  Consensus statement on the diagnosis of multiple system atrophy. J Neurol Sci 1999;16394- 98
PubMedArticle
3.
Gilman  SLittle  RJohanns  J  et al.  Evolution of sporadic olivopontocerebellar atrophy into multiple system atrophy. Neurology 2000;55527- 532
PubMedArticle
4.
Quinn  NDaniel  S Differences between multiple system atrophy and olivopontocerebellar atrophy. Ann Neurol 1996;40945- 946
PubMedArticle
5.
Penney  J Multiple system atrophy and nonfamilial olivopontocerebellar atrophy are the same disease. Ann Neurol 1995;37553- 554
PubMedArticle
6.
Rinne  JOBurn  DJMathias  CJQuinn  NPMarsden  CDBrooks  DJ Positron emission tomography studies on the dopaminergic system and striatal opioid binding in the olivopontocerebellar atrophy variant of multiple system atrophy. Ann Neurol 1995;37568- 573
PubMedArticle
7.
Schrag  AKingsley  DPhatouras  C  et al.  Clinical usefulness of magnetic resonance imaging in multiple system atrophy. J Neurol Neurosurg Psychiatry 1998;6565- 71
PubMedArticle
8.
Kraft  ESchwarz  JTrenkwalder  CVogl  TPfluger  TOertel  W The combination of hypointense and hyperintense signal changes on T2-weighted magnetic resonance imaging sequences. Arch Neurol 1999;56225- 228
PubMedArticle
9.
Murata  YYamaguchi  SKawakami  H  et al.  Characteristic magnetic resonance imaging in Machado-Joseph disease. Arch Neurol 1998;5533- 37
PubMedArticle
10.
Bürk  KSkalej  MDichgans  J Pontine MRI hyperintensities (“the cross sign”) are not pathognomonic for multiple system atrophy (MSA) [case report]. Mov Disord 2001;16535
PubMedArticle
11.
Counsell  CHughes  A Clinical usefulness of MRI in multisystem atrophy [letter]. J Neurol Neurosurg Psychiatry 1999;66694
PubMedArticle
12.
Klockgether  TSchroth  GDiener  HCDichgans  J Idiopathic cerebellar ataxia of late onset: natural history and MRI morphology. J Neurol Neurosurg Psychiatry 1990;53297- 305
PubMedArticle
13.
Eardley  IQuinn  NPFowler  CJ  et al.  The value of urethral sphincter electromyography in the differential diagnosis of parkinsonism. Br J Urol 1989;64360- 362
PubMedArticle
14.
Brooks  DJIbanez  VSawle  GV  et al.  Striatal D2 receptor status in patients with Parkinson's disease, striatonigral degeneration, and progressive supranuclear palsy, measured with 11C-raclopride and positron emission tomography. Ann Neurol 1992;31184- 192
PubMedArticle
15.
Savoiardo  MStrada  LGirotti  F Olivopontocerebellar atrophy: MR diagnosis and relationship to multiple system atrophy. Radiology 1990;174693- 696
PubMedArticle
16.
Lantos  PLPapp  MI Cellular pathology of multiple system atrophy: a review. J Neurol Neurosurg Psychiatry 1994;57129- 133
PubMedArticle
17.
Papp  MIKahn  JELantos  P Glial cytoplasmic inclusions in the CNS of patients with multiple system atrophy (striatonigral degeneration, olivopontocerebellar atrophy and Shy-Drager syndrome). J Neurol Sci 1989;9479- 100
PubMedArticle
18.
Quinn  N Multiple system atrophy: the nature of the beast. J Neurol Neurosurg Psychiatry 1989;(suppl)78- 79
PubMed
19.
Milton  WJAtlas  SWLexa  FJMozley  PDGur  RE Deep grey matter hypointensity patterns with aging in healthy adults: MRI imaging at 1.5 T. Radiology 1991;181715- 719
PubMedArticle
Original Contribution
June 2005

Clinical and Magnetic Resonance Imaging Characteristics of Sporadic Cerebellar Ataxia

Author Affiliations

Author Affiliations: Department of Neurology, University of Ulm, Ulm (Dr Bürk); Departments of Neurology (Drs Bürk, Schulz, and Dichgans) and Neuroradiology (Dr Bühring), University of Tübingen, Tübingen; and Institute of Human Genetics, University of Lübeck, Lübeck (Drs Zühlke and Hellenbroich), Germany.

Arch Neurol. 2005;62(6):981-985. doi:10.1001/archneur.62.6.981
Abstract

Background  It is unknown whether multiple system atrophy of the cerebellar type (MSA-C) and idiopathic cerebellar ataxia with extracerebellar presentation (IDCA-P) represent distinct entities.

Objective  To investigate the discriminative validity of magnetic resonance imaging in sporadic cerebellar ataxia.

Design  Basal ganglia and infratentorial structures were screened for signal abnormalities and atrophic changes. Magnetic resonance imaging raters were masked to the clinical diagnosis.

Setting  Outpatient clinic of a university hospital.

Patients  Forty-one individuals were diagnosed as having MSA-C (n = 30) or IDCA-P (n = 11) based on their clinical features.

Results  Shrinkage of the cerebellar vermis and hemispheres was found in both groups. Atrophy of the brainstem and middle cerebellar peduncles was significantly more frequent in patients with MSA-C (P<.001). Hyperintensities of infratentorial structures were common in patients with MSA-C (middle cerebellar peduncles: 87%; pons: 97%) but were absent in patients with IDCA-P. Hypointensities or hyperintensities of basal ganglia structures did not reliably differentiate the groups.

Conclusions  Patients with MSA-C were characterized by a higher frequency and severity of magnetic resonance imaging abnormalities (atrophic changes and additional hyperintense signal changes) of the middle cerebellar peduncles and pons. The presence of these magnetic resonance imaging features points to the diagnosis of MSA-C and helps differentiate MSA-C from other types of sporadic cerebellar ataxia with extracerebellar features.

The term sporadic cerebellar ataxia comprises a variety of nonhereditary cerebellar syndromes of unknown origin. Neuropathologic features vary from isolated cerebellar degeneration to combined neuronal degeneration and gliosis in the inferior olives, pons, and cerebellum (olivopontocerebellar atrophy).1 Clinically, patients may have a purely cerebellar syndrome (idiopathic cerebellar ataxia [IDCA-C]) or additional extracerebellar features (IDCA-P).

Combined cerebellar and pontine atrophy is also a neuropathologic hallmark of multiple system atrophy (MSA), a sporadic and unrelentlessly progressive neurodegenerative disorder that leads to incapacity and a reduced life expectancy. Apart from glial cytoplasmic inclusions, neuropathologic changes are not restricted to the inferior olives, pontine nuclei, and Purkinje cells in MSA brains but may also be found in the putamen, caudate nucleus, substantia nigra, and autonomic nuclei of the brainstem and in the intermediolateral cell columns in the spinal cord.2 Clinically, MSA is associated with various combinations of cerebellar ataxia, basal ganglia symptoms, and severe autonomic dysfunction.2 Many patients with MSA initially develop basal ganglia symptoms (MSA of the striatonigral type [MSA-P]), whereas others start with a cerebellar syndrome (MSA of the cerebellar type [MSA-C]). The question of whether MSA-C and IDCA-P represent the same disease has been discussed controversially in the literature.1,36 However, the neuropathologic proof of this hypothesis has not yet been established.

Modern imaging techniques allow morphologic studies of central nervous system structures in vivo. The presence of putaminal and infratentorial signal changes has been considered to be predictive of the diagnosis of MSA-P with respect to Parkinson disease and other basal ganglia disorders.7,8 Infratentorial signal changes, especially cruciform signal abnormalities in the pons on T2- and proton-weighted magnetic resonance images (MRIs) (the “cross sign”) that are thought to result from degeneration of pontine neurons and transverse pontocerebellar fibers, have been claimed to be highly predictive of the diagnosis of MSA. On the other hand, these signal abnormalities have been documented in several types of hereditary olivopontocerebellar atrophy.9,10 The predictive value of qualitative variables has, therefore, been questioned.11

The present study was undertaken to investigate the discriminative validity of MRI signal changes in various types of sporadic cerebellar ataxia. To address this question, basal ganglia and infratentorial structures were screened for the presence of hypointense and hyperintense MRI signal abnormalities and atrophic changes in 41 patients with sporadic cerebellar ataxia. Individuals were diagnosed as having MSA-C or IDCA-P based on their clinical features.

METHODS
PATIENTS

To investigate the differentiation of MSA-C and IDCA-P in patients with cerebellar symptoms with clinical presentations as similar as possible, those with evidence of cognitive impairment were excluded from the study (dementia has to be absent in MSA according to the Guideline of the International Consensus Statement of MSA2). Forty-six patients with cerebellar symptoms (mean ± SD age, 60.5 ± 7.2 years; age range, 41-75 years; mean ± SD age at onset, 54.8 ± 8.5 years; age range at onset, 30-70 years; mean ± SD disease duration, 5.7 ± 3.6 years; range of disease duration, 1-19 years) fulfilled the following inclusion criteria: (1) chronic progressive cerebellar dysfunction; (2) disease onset after age 35 years (patients who were younger at onset were excluded because MSA-C usually starts after age 35 years2); (3) the absence of any neurodegenerative disorders in relatives, no evidence of consanguinity of parents, and negative molecular genetic testing for Friedreich ataxia and spinocerebellar ataxia types 1, 2, 3, and 6; and (4) the exclusion of symptomatic causes of ataxia, such as gluten sensitivity, infectious disease, multiple sclerosis, paraneoplastic disease, disease of the thyroid, Wilson disease, hypovitaminosis, alcoholism, chronic anticonvulsive therapy, ischemia, or neoplasm.

CLINICAL RATING

Individuals were examined using a standardized examination procedure. The severity of the cerebellar symptoms was rated on a scale from 0 (absent) to 5 (most severe).12 Age at onset was defined as the age at which the onset of motor symptoms was experienced by the patient.

CLASSIFICATION

Patients were separated into the following diagnostic categories:

  • Multiple system atrophy of the cerebellar type (MSA-C): Patients fulfilling the modified criteria of the International Consensus Statement of MSA2: cerebellar ataxia with additional severe autonomic failure or a parkinsonian syndrome unresponsive or poorly responsive to levodopa therapy. Severe autonomic failure was diagnosed based on the presence of postural hypotension (orthostatic decline of ≥30 mm Hg in systolic blood pressure immediately [0 minutes] after having been supine for 5 minutes and 3 minutes after assumption of the upright position). Diagnosis of the parkinsonian syndrome required at least 2 of the following features: akinesia, rigidity, tremor, and poor or no response to levodopa therapy. The finding of dementia or limited gaze excluded the diagnosis of MSA-C.

  • Cerebellar ataxia with additional extracerebellar features (IDCA-P): Patients with extracerebellar symptoms who did not fulfill the criteria for MSA, in particular without autonomic failure.

MRI STUDIES

All MRI measurements were performed using a 1.5-T scanner (Magnetom Vision; Siemens AG, Erlangen, Germany) with a standard head coil. Two MRI series were acquired. We scanned a 3-dimensional Fourier transform fast low-angle shot sequence that produced isotropic T1-contrasted image sets in high resolution (repetition time, 15 milliseconds; echo time, 5 milliseconds; flip angle, 30°; number of excitations, 1; section thickness, 0.9 mm; and pixel size, 0.9 × 0.9 mm). A double-contrast 2-dimensional Fourier transform turbo spin echo was acquired twice in interleaved section positions to obtain a gapless set of images (repetition time, 5800 milliseconds; echo time, 15/75 milliseconds; number of excitations, 2; section thickness, 2 mm; gap, 2 mm; and pixel size, 0.9 × 0.9 mm).

Fast low-angle shot images were used for cerebellar and brainstem abnormalities, and signal changes were rated on T2-weighted images. Anonymous images were evaluated independently by 2 experienced raters (K.B. and U.B.). In cases of differing evaluations, the images were reanalyzed by both raters and consensus was reached. Qualitative and semiquantitative analyses of central nervous system structures were performed visually.

T2-weighted axial MRIs were screened for the presence of (1) signal hypointensity of the dentate nucleus, (2) signal hypointensity of the substantia nigra, (3) signal hypointensity of the red nucleus, (4) signal hyperintensities along the lateral boundary of the putamen, (5) signal hyperintensities along the medial boundary of the putamen, and (6) signal hypointensities of the putamen (defined as areas of signal intensity equal to or lower than the signal intensity of the globus pallidus).

The extent of the following variables was assessed semiquantitatively by applying scores of absent (score 0), mild (score 1), moderate (score 2), and severe (score 3): cruciform signal hyperintensities in the pons (the cross sign) and signal hyperintensities in the middle cerebellar peduncles on T2-weighted axial images; atrophy of the cerebellar vermis, atrophy of the cerebellar hemispheres, and atrophy of the brainstem on T1-weighted sagittal images; and atrophy of the middle cerebellar peduncles on T1-weighted axial images.

STATISTICAL ANALYSIS

A software package (JMP; SAS Institute Inc, Cary, NC) was used for statistical analysis. Statistical comparisons of clinical and qualitative MRI variables were conducted using χ2 tests. The analysis of semiquantitative variables was performed using analysis of variance (ANOVA). Post hoc paired-group comparisons were explored using the Tukey test or, in the case of nonparametric distribution, the Wilcoxon rank sum test. Differences were considered statistically significant at P < .05. For correlation studies of disability and semiquantitative MRI scores, Spearman rho was applied. To achieve a global significance level of 5%, P values were corrected by applying the modified Bonferroni-Holm adjustment.

RESULTS
PATIENT CHARACTERISTICS

Thirty patients fulfilled the diagnostic criteria for MSA-C. Eleven patients had extracerebellar features that did not correspond to the diagnostic criteria of MSA-C. The characteristics and clinical features of the patients are given in Table 1. The mean age at clinical examination differed between groups, with patients with MSA-C being older than those with IDCA-P (ANOVA: F1,39 = 4.2996; P = .04). Patients with MSA-C were also significantly older at the perceived onset of motor symptoms than those with IDCA-P (ANOVA: F1,39 = 11.3780; P = .002). In patients with IDCA-P, the mean disease duration was significantly longer than in those with MSA-C (ANOVA: F1, 39 = 7.5693; P = .009).

CLINICAL FEATURES

All patients had ataxia of stance, gait, and limbs and dysarthria (Table 1). Although impaired smooth pursuit and gaze-evoked nystagmus were present in both cerebellar groups, spontaneous nystagmus was uncommon in MSA-C. Autonomic dysfunction (bladder dysfunction, sleep behavior disorders, and constipation) was a characteristic finding in the MSA-C group but could also been found in the IDCA-P group. Pyramidal tract signs and sensory deficits were found in both groups.

MRI VARIABLES
Qualitative Analysis

Shrinkage of the cerebellar vermis and hemispheres was found in both groups. Atrophy of the brainstem and middle cerebellar peduncles was statistically significantly more frequent in patients with MSA-C than in those with IDCA-P (Table 2). Nearly all patients with MSA-C showed hyperintensities of the middle cerebellar peduncles and pons, whereas these features were absent in individuals clinically diagnosed as having IDCA-P. Signal reduction was found in approximately half of the patients with MSA-C but not in those with IDCA-P. Hypointensities of the red nucleus, substantia nigra, and putamen and hyperintensities of the medial putaminal border occurred in a small proportion of patients with MSA-C. The distribution of hyperintensities of the lateral parts of the putamen did not differ between groups. In a single patient with MSA-C, there was evidence of additional atrophy of the cervical spinal cord.

Semiquantitative Analysis

Analysis of semiquantitative variables yielded significant group differences between MSA-P and IDCA-P for the vermis (ANOVA: F1,39 = 3.5061; P = .07), hemispheres (ANOVA: F1,39 = 4.6923; P = .04), brainstem (ANOVA: F1,39 = 78.5212; P<.001), and middle cerebellar peduncles (ANOVA: F1,39 = 32.8775; P<.001). Group differences were even more pronounced for the comparison of T2 hyperintensities of infratentorial structures (ANOVA: pons, F1,39 = 50.1381; and middle cerebellar peduncles, F1,39 = 27.5202; P<.001 for both).

The rating scores for the degree of both cerebellar structures were higher for patients with MSA-C (vermis: median, 2; range, 1-3; hemispheres: median, 2; range, 0-3) than for those with IDCA-P (vermis: median, 1; range, 0-3; hemispheres: median, 1; range, 0-3) (vermis: P = .13; hemispheres: P = .03). Higher rating scores were also obtained in patients with MSA-C for atrophy of the brainstem (MSA-C: median, 2; range, 1-3; IDCA-P: median, 0; range, 0-1; P<.001) and middle cerebellar peduncles (MSA-C: median, 2; range, 0-3; IDCA-P: median, 0; range, 0-1; P<.001). Median scores of hyperintensities in the pons and middle cerebellar peduncles were 1.5 (range, 0-3) in patients with MSA-C. The latter signal abnormalities were not documented in patients with IDCA-P. Therefore, group differences were highly significant for these 2 variables (P<.001 for both).

Correlation Studies

There was a statistically significant positive correlation between disability and semiquantitative MRI scores for all anatomic structures studied (Table 3). Putaminal signal abnormalities were positively correlated with rigor and akinesia (Table 4).

Examples of MRI Findings

The Figure shows characteristic findings with atrophy of the brainstem and middle cerebellar peduncles, with additional signal hyperintensities on T2-weighted MRIs in patients with MSA-C.

COMMENT

It had been a matter of a long-standing discussion whether IDCA-P represents a variation of MSA-C.1,36 In the literature, it is commonly assumed that not all cerebellar disorders with extracerebellar symptoms will evolve to MSA-C3 despite the fact that the final neuropathologic proof for the existence of at least 2 independent disorders is still lacking. Gilman et al3 estimated that approximately 25% of patients with sporadic ataxia with extracerebellar involvement will develop MSA-C within 5 years of the onset of cerebellar symptoms. The predictive validity of any clinical or functional characteristics has not been established to date. Electromyographic evidence of chronic reinnervation of the external sphincter has been recommended to support the diagnosis of MSA,13 but its validity in MSA-C still remains to be established. Positron emission tomography studies may provide evidence of reduced dopamine D2 receptor density, thus reflecting degeneration of striatal neurons in MSA.14 These investigations, however, require extensive technical prerequisites and are not necessarily significant in all patients with MSA.

The present MRI analysis thus gives further support to the hypothesis that MSA-C and IDCA-P represent distinct neurodegenerative disorders because patients with cerebellar symptoms clinically diagnosed as having IDCA-P and MSA-C were shown to be characterized by distinct MRI features. There was substantial cerebellar atrophy in both groups, whereas atrophy of the brainstem and middle cerebellar peduncles was found to be more frequent and more pronounced in patients with MSA-C. In patients with MSA-C, infratentorial atrophy was typically associated with signal hyperintensities in the pons and middle cerebellar peduncles. Similar abnormalities were first described by Savoiardo et al15 in a heterogeneous group of sporadic and hereditary ataxias. Pontine cruciform signal changes are thought to be contingent on differential involvement of pontocerebellar and pyramidal tract fibers in MSA with depletion of pontine neurons and crossing myelinated transverse pontocerebellar fibers and preservation of the fibers of the corticospinal tract running craniocaudally.7 Their presence seems to be a predictor of the diagnosis of MSA-C. On the other hand, this cross sign should not be considered pathognomonic because it has also been described in autosomal dominant spinocerebellar ataxias.9

Basal ganglia signal abnormalities were restricted to a single patient with MSA-C, a finding that is consistent with neuropathologic and clinical MSA-C features.1618 The presence of striatal, cerebellar, and brainstem abnormalities had already been postulated to be helpful to differentiate MSA-P from Parkinson disease,7,8 but Schrag et al7 also reported normal MRI findings in up to 20% of patients with MSA-P. In addition, hypointense signal abnormalities in the putamen on T2-weighted images were found to be age-related findings in healthy individuals.19 Regarding the low prevalence of basal ganglia abnormalities even in patients with MSA-C with additional basal ganglia symptoms, the absence of these signal abnormalities does not necessarily exclude MSA-C.

Patients with MSA-C are characterized by a higher frequency and severity of MRI abnormalities of the middle cerebellar peduncles and pons. These features consist of atrophic changes with additional hyperintense signal abnormalities. The presence of such MRI features points to the diagnosis of MSA-C. Nevertheless, the validity of these MRI criteria need to be established in future postmortem studies.

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Article Information

Correspondence: Katrin Bürk, MD, Institute of Brain Research, University of Tübingen, Calwerstr 3, D-72076 Tübingen, Germany (buerk@ngi.de).

Accepted for Publication: November 8, 2004.

Author Contributions:Study concept and design: Bürk and Schulz. Acquisition of data: Bürk, Bühring, Zühlke, and Hellenbroich. Analysis and interpretation of data: Bürk, Bühring, Schulz, and Dichgans. Drafting of the manuscript: Bürk, Bühring, Zühlke, and Dichgans. Critical revision of the manuscript for important intellectual content: Bürk, Bühring, Schulz, Hellenbroich, and Dichgans. Statistical analysis: Bürk and Schulz. Administrative, technical, and material support: Bühring, Zühlke, and Hellenbroich. Study supervision: Schulz and Dichgans.

References
1.
Gilman  SQuinn  NP The relationship of multiple system atrophy to sporadic olivopontocerebellar atrophy and other forms of idiopathic late onset cerebellar atrophy. Neurology 1996;461197- 1199
PubMedArticle
2.
Gilman  SLow  PAQuinn  N  et al.  Consensus statement on the diagnosis of multiple system atrophy. J Neurol Sci 1999;16394- 98
PubMedArticle
3.
Gilman  SLittle  RJohanns  J  et al.  Evolution of sporadic olivopontocerebellar atrophy into multiple system atrophy. Neurology 2000;55527- 532
PubMedArticle
4.
Quinn  NDaniel  S Differences between multiple system atrophy and olivopontocerebellar atrophy. Ann Neurol 1996;40945- 946
PubMedArticle
5.
Penney  J Multiple system atrophy and nonfamilial olivopontocerebellar atrophy are the same disease. Ann Neurol 1995;37553- 554
PubMedArticle
6.
Rinne  JOBurn  DJMathias  CJQuinn  NPMarsden  CDBrooks  DJ Positron emission tomography studies on the dopaminergic system and striatal opioid binding in the olivopontocerebellar atrophy variant of multiple system atrophy. Ann Neurol 1995;37568- 573
PubMedArticle
7.
Schrag  AKingsley  DPhatouras  C  et al.  Clinical usefulness of magnetic resonance imaging in multiple system atrophy. J Neurol Neurosurg Psychiatry 1998;6565- 71
PubMedArticle
8.
Kraft  ESchwarz  JTrenkwalder  CVogl  TPfluger  TOertel  W The combination of hypointense and hyperintense signal changes on T2-weighted magnetic resonance imaging sequences. Arch Neurol 1999;56225- 228
PubMedArticle
9.
Murata  YYamaguchi  SKawakami  H  et al.  Characteristic magnetic resonance imaging in Machado-Joseph disease. Arch Neurol 1998;5533- 37
PubMedArticle
10.
Bürk  KSkalej  MDichgans  J Pontine MRI hyperintensities (“the cross sign”) are not pathognomonic for multiple system atrophy (MSA) [case report]. Mov Disord 2001;16535
PubMedArticle
11.
Counsell  CHughes  A Clinical usefulness of MRI in multisystem atrophy [letter]. J Neurol Neurosurg Psychiatry 1999;66694
PubMedArticle
12.
Klockgether  TSchroth  GDiener  HCDichgans  J Idiopathic cerebellar ataxia of late onset: natural history and MRI morphology. J Neurol Neurosurg Psychiatry 1990;53297- 305
PubMedArticle
13.
Eardley  IQuinn  NPFowler  CJ  et al.  The value of urethral sphincter electromyography in the differential diagnosis of parkinsonism. Br J Urol 1989;64360- 362
PubMedArticle
14.
Brooks  DJIbanez  VSawle  GV  et al.  Striatal D2 receptor status in patients with Parkinson's disease, striatonigral degeneration, and progressive supranuclear palsy, measured with 11C-raclopride and positron emission tomography. Ann Neurol 1992;31184- 192
PubMedArticle
15.
Savoiardo  MStrada  LGirotti  F Olivopontocerebellar atrophy: MR diagnosis and relationship to multiple system atrophy. Radiology 1990;174693- 696
PubMedArticle
16.
Lantos  PLPapp  MI Cellular pathology of multiple system atrophy: a review. J Neurol Neurosurg Psychiatry 1994;57129- 133
PubMedArticle
17.
Papp  MIKahn  JELantos  P Glial cytoplasmic inclusions in the CNS of patients with multiple system atrophy (striatonigral degeneration, olivopontocerebellar atrophy and Shy-Drager syndrome). J Neurol Sci 1989;9479- 100
PubMedArticle
18.
Quinn  N Multiple system atrophy: the nature of the beast. J Neurol Neurosurg Psychiatry 1989;(suppl)78- 79
PubMed
19.
Milton  WJAtlas  SWLexa  FJMozley  PDGur  RE Deep grey matter hypointensity patterns with aging in healthy adults: MRI imaging at 1.5 T. Radiology 1991;181715- 719
PubMedArticle
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