DOI: 10.1148/radiol.2393050459
(Radiology 2006;239:825-830.)
© RSNA, 2006
MR Imaging of Middle Cerebellar Peduncle Width: Differentiation of Multiple System Atrophy from Parkinson Disease1
Giuseppe Nicoletti, MD,
Francesco Fera, MD,
Francesca Condino, PhD,
William Auteri, MD,
Olivier Gallo, STc,
Pierfrancesco Pugliese, MD,
Gennarina Arabia, MD,
Letterio Morgante, MD,
Paolo Barone, MD,
Mario Zappia, MD and
Aldo Quattrone, MD
1 From the Institute of Neurological Sciences, National Research Council, Mangone, Cosenza, Italy (G.N., F.F., F.C., O.G., M.Z., A.Q.); Department of Neurosciences, Azienda Ospedaliera, Cosenza, Italy (W.A.); Institute of Neurology, University Magna Graecia, Catanzaro, Italy (P.P., G.A., M.Z., A.Q.); Department of Neuroscience, Psychiatry and Anesthesiology, University of Messina, Policlinico Universitario, Messina, Italy (L.M.); and Department of Neurological Sciences, University Federico II, Naples, Italy (P.B.). Received March 17, 2005; revision requested May 10; revision received June 23; accepted July 20; final version accepted September 6.
Address correspondence to A.Q., Clinica Neurologica, Policlinico Universitario Campus di Germaneto, 88100 Catanzaro, Italy (e-mail: a.quattrone{at}isn.cnr.it).
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ABSTRACT
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Purpose: To prospectively assess if middle cerebellar peduncle (MCP) atrophy, evaluated at magnetic resonance (MR) imaging, can help differentiate multiple system atrophy (MSA) from Parkinson disease (PD).
Materials and Methods: All participants provided informed consent for participation in the study, which was approved by the institutional review board. Sixteen consecutive patients with MSA, 26 consecutive patients with PD, and 14 healthy control subjects were examined with MR imaging. Images were interpreted independently by two experienced neuroradiologists blinded to clinical information, who visually inspected the images for the presence or absence of putaminal atrophy, putaminal hypointensity, slitlike hyperintensity in the posterolateral margin of the putamen, brainstem atrophy, hyperintensity of the MCP, and cruciform hyperintensity of the pons. Measurements of MCP width on T1-weighted volumetric spoiled gradient-echo images were performed in all subjects. Differences in MCP width among the groups were evaluated by using the Kruskall-Wallis test, followed by the Mann-Whitney U test for multiple comparisons and Bonferroni correction.
Results: All patients (mean age, 63.88 years; range, 55–72 years) with MSA had at least one of the features commonly observed in this disease on MR images, whereas control subjects (mean age, 66.93 years; range, 61–77 years) and all but one patient with PD (mean age, 65.31 years; range, 51–79 years) had normal MR images. The average MCP width was significantly smaller in patients with MSA (6.10 mm ± 1.18 [standard deviation]) than in those with PD (9.32 mm ± 0.77, P < .001) or control subjects (9.80 mm ± 0.66, P < .001).
Conclusion: Measurement of MCP width on MR images may be useful for distinguishing patients with MSA from those with PD.
© RSNA, 2006
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INTRODUCTION
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Multiple system atrophy (MSA) is a neurodegenerative disorder often confused with Parkinson disease (PD). Patients with MSA commonly exhibit the clinical signs of parkinsonism, and up to 30% respond to levodopa in a short-term period (1). Two major motor manifestations can be distinguished clinically. Parkinsonian features predominate in 80% of patients with MSA, and cerebellar ataxia is the main motor feature in 20% of patients with MSA (2). In addition to clinical criteria, modern imaging methods such as magnetic resonance (MR) imaging, single-photon emission computed tomography, and positron emission tomography are increasingly used to differentiate patients with MSA from those with PD (3–9). Despite recent progress in neuroimaging, however, differentiation of MSA from PD may be difficult, mainly in the early stages of MSA with parkinsonian features owing to several overlapping features such as rest tremor or asymmetric akinesia and rigidity.
In MSA there is neuronal loss and gliosis in the inferior olives, pons, cerebellum, substantia nigra, locus ceruleus, striatum, and intermediolateral column of the spinal cord (10). In MSA with parkinsonian features, the nigrostriatal system is the main site of disease, but less severe degeneration can be widespread and normally includes the olivopontocerebellar system (10,11). In MSA with cerebellar ataxia, the olivopontocerebellar system is mainly involved, along with loss of pontine neurons and transverse pontocerebellar fibers and atrophy of middle cerebellar peduncles (MCPs) (10,11).
In parkinsonian syndromes, the measurement of MCP width on MR images has not been reported, to our knowledge. Thus, the purpose of our study was to prospectively assess if MCP atrophy, evaluated at MR imaging, can help differentiate MSA from PD.
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MATERIALS AND METHODS
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Patients and Control Subjects
From June 2002 to July 2004, 16 consecutive patients with MSA, 26 consecutive patients with PD, and 14 healthy control subjects were included in our study. Clinical diagnoses of PD and MSA were made by one of the authors (G.N., with 10 years of experience in movement disorders) according to established criteria (12,13). All patients were evaluated clinically, tested for levodopa response, and examined with MR imaging. The levodopa response was considered good when the clinical improvement was 30% or greater and moderate when the clinical improvement was 20% or greater in respect to baseline condition. None of the control subjects had a history of neurologic or psychiatric diseases. All control subjects underwent brain MR imaging. All participants provided informed consent for participation in the study, which was approved by the institutional review board.
MR Imaging Protocol
Brain MR imaging was performed according to our routine protocol by using a 1.5-T imager (Signa NV/I; GE Medical Systems, Milwaukee, Wis). All MR examinations included transverse intermediate-weighted/T2-weighted dual-echo fast spin-echo (repetition time msec/echo time msec, 3500/10.2, 85; section thickness, 4 mm; frequency- and phase-encoding matrix, 288 x 224), transverse fluid-attenuated inversion recovery (repetition time msec/echo time msec/inversion time msec, 8000/120/2000; section thickness, 4 mm; frequency- and phase-encoding matrix, 256 x 224), transverse T2-weighted gradient-echo (500/15; section thickness, 4 mm; frequency- and phase-encoding matrix, 256 x 192; flip angle, 20°), and T1-weighted volumetric spoiled gradient-echo (15.2/6.8; section thickness, 0.6 mm; frequency- and phase-encoding matrix, 256 x 256; flip angle, 15°) images.
Image Analysis
Two independent raters (F.F. and W.A.) whose experience in neuroradiology ranged from 10 to 20 years and who were blinded to the patients' diagnosis qualitatively evaluated all MR images. To assess the intrarater reliability, a second evaluation was made 2 weeks after (images in a different order) the first evaluation by the two neuroradiologists, who scored all the images blindly and independently.
Conventional transverse brain MR images were visually inspected for the presence or absence of putaminal atrophy, putaminal hypointensity, slitlike hyperintensity in the posterolateral margin of the putamen, brainstem atrophy, hyperintensity of the MCP, and cruciform hyperintensity of the pons ("hot cross bun" sign). Putaminal hypointensity and slitlike hyperintensity in the posterolateral margin of the putamen were evaluated on T2-weighted images. Cruciform hyperintensity was considered present if it was unequivocal on T2-weighted images. Anteroposterior midbrain diameter on transverse T2-weighted MR images was also measured. Measurement of MCP width was performed on sagittal T1-weighted volumetric spoiled gradient-echo images with the aid of a multiplanar reconstruction program (GE Medical Systems). For the measurement of MCP, the midsagittal MR section of the brain was chosen as the reference starting view. Left and right MCPs were identified on the parasagittal view that best exposed the MCP between the pons and the cerebellum; the linear distance between the superior and inferior borders of the MCP, as delimited by the peripeduncular cerebrospinal fluid spaces of pontocerebellar cisterns, was measured. Each MCP (left and right) was measured, and a mean value for the two MCPs was calculated.
Clinical Features
All patients provided a detailed medical history and underwent neurologic examination performed by one of the authors (G.N.) with experience in movement disorders. The following clinical characteristics were assessed: age at onset, duration, and severity of the disease measured with both Hoehn and Yahr Rating Scale and Unified Parkinson Disease Rating Scale and response to acute administration of levodopa. The age at the examination and sex of all participants were also recorded.
Statistical Analysis
The difference in sex distribution between patients with MSA, patients with PD, and control subjects was evaluated with the 
2 test, while the age at examination was evaluated with a one-way analysis of variance. To compare the clinical features between MSA and PD, an unpaired t test was used for continuous variables and the Mann-Whitney U test was used for discrete variables. The Kruskall-Wallis test was used to evaluate differences in MCP width among all groups, followed by the Mann-Whitney U test for multiple comparisons; the resulting P values were corrected according to Bonferroni. The interrater and intrarater reliability between the two readers and the difference between right and left MCP for the same reader were assessed with the Spearman correlation coefficient. Sensitivity, specificity, and positive predictive value for differentiating MSA from PD were calculated for the MCP measurements by using the optimal cutoff values determined with receiver operating characteristic curve analysis (14). Moreover, these validity measures were calculated for abnormal findings on routine MR images.
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RESULTS
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Demographic and Clinical Data
At the onset of the disease, 13 patients with MSA had features of parkinsonism and autonomic dysfunction and three exhibited cerebellar signs such as ataxia, but all MSA patients showed a combination of parkinsonian, autonomic, cerebellar, and pyramidal signs at the time of the current study. All patients with PD had a good levodopa response, whereas only four of 16 patients with MSA had a moderate levodopa response. There was no difference in age at the time of examination (P = .470) between patients with PD (mean, 65.31 years ± 7.48 [standard deviation]; range, 51–79 years) and those with MSA (mean, 63.88 years ± 5.56; range, 55–72 years) and the control subjects (mean, 66.93 years ± 6.50; range, 61–77 years). There was no difference in disease duration (P = .626) between patients with PD (mean, 5.92 years ± 6.46) and those with MSA (mean, 5.06 years ± 3.38). There was no difference in age at onset of disease(P = .848) between patients with MSA (mean, 58.81 years ± 6.36; range, 47–69 years) and those with PD (mean, 59.38 years ± 10.77; range, 33–78 years) (Table 1).
Imaging Features
The mean anteroposterior midbrain diameter did not differ significantly among the different groups (MSA, 16.05 mm ± 0.70; PD, 15.95 mm ± 0.71; control subjects, 16.22 mm ± 0.22; P = .107). In all MSA patients, MR images showed at least one of the features commonly described in this disease (3,15–17), while MR images were normal in all but one patient with PD (Fig 1, Table 2). Among 16 MSA patients, eight had cruciform hyperintensity, nine had slitlike hyperintensity of the posterolateral margin of the putamen, five had atrophy of the putamen, six had putaminal hypointensity, five had brainstem atrophy, and two had hyperintensity of the MCPs (Table 2). There was a significant difference (P = .009) in disease duration between MSA patients with (7.0 years ± 3.6) and those without (3.13 years ± 1.73) this latter MR feature.
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Figure 1a: Sagittal T1-weighted volumetric spoiled gradient-echo (15.2/6.8) MR images show MCP width (arrow) in a (a) control subject (MCP width, 8.9 mm), (b) PD patient (MCP width, 8.5 mm), (c) MSA patient without cruciform hyperintensity (MCP width, 7.1 mm), and (d) MSA patient with cruciform hyperintensity (MCP width, 5.8 mm).
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Figure 1b: Sagittal T1-weighted volumetric spoiled gradient-echo (15.2/6.8) MR images show MCP width (arrow) in a (a) control subject (MCP width, 8.9 mm), (b) PD patient (MCP width, 8.5 mm), (c) MSA patient without cruciform hyperintensity (MCP width, 7.1 mm), and (d) MSA patient with cruciform hyperintensity (MCP width, 5.8 mm).
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Figure 1c: Sagittal T1-weighted volumetric spoiled gradient-echo (15.2/6.8) MR images show MCP width (arrow) in a (a) control subject (MCP width, 8.9 mm), (b) PD patient (MCP width, 8.5 mm), (c) MSA patient without cruciform hyperintensity (MCP width, 7.1 mm), and (d) MSA patient with cruciform hyperintensity (MCP width, 5.8 mm).
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Figure 1d: Sagittal T1-weighted volumetric spoiled gradient-echo (15.2/6.8) MR images show MCP width (arrow) in a (a) control subject (MCP width, 8.9 mm), (b) PD patient (MCP width, 8.5 mm), (c) MSA patient without cruciform hyperintensity (MCP width, 7.1 mm), and (d) MSA patient with cruciform hyperintensity (MCP width, 5.8 mm).
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With regard to MCP width, the right and left MCPs did not show any difference in all groups considered (Table 2). No significant difference was observed between men and women in all groups. The intrarater reliability of left MCP was 0.922 for the first reader and 0.957 for the second reader. The interrater reliability of the measurement procedure was 0.985 for the right MCP and 0.973 for the left MCP. The correlation coefficient between the values recorded for the left and right MCPs was 0.968 for the first reader and 0.956 for the second. In MSA patients, the average width of the MCP (6.10 mm ± 1.18) was significantly smaller than that observed in PD patients (9.32 mm ± 0.77, P < .001) or control subjects (9.80 mm ± 0.66, P < .001). Moreover, none of the MCP widths detected in the MSA group surpassed the lowest MCP width observed in the PD or control group (Fig 2). In MSA patients with cruciform hyperintensity, the MCP width was significantly lower (5.29 mm ± 0.75) than that observed in MSA patients without this MR sign (6.92 mm ± 0.96, P = .006).
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Figure 2: Box plot of the MCP widths obtained in patients with MSA and PD and in control subjects. Note that none of the MCP measurements in the MSA group reached the lowest value obtained in PD patients or control subjects. Vertical solid lines (whiskers) show lower and upper MCP width. Box stretches from lower hinge (25th percentile) to upper hinge (75th percentile); median is shown as line across each box.
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Statistical Measures
Sensitivity (proportion of patients with MSA with abnormal MR findings), specificity (proportion of patients with PD or control subjects with normal MR parameters), and positive predictive value (likelihood of a person with abnormal MR findings to have MSA) of MCP width, putaminal hypointensity, putaminal slitlike hyperintensity, and cruciform hyperintensity were calculated with receiver operating characteristic curve analysis. The sensitivity of MCP width measurements on MR images to distinguish MSA from PD was 100% by using a cutoff of 8.0 mm or less. The specificity of the method to differentiate between MSA and PD was 100%. The positive predictive value of the MCP diameters was 100% (MSA vs PD) (Table 3).
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DISCUSSION
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MSA is an adult-onset, sporadic, progressive neurodegenerative disease of unknown cause with signs or symptoms in extrapiramidal, pyramidal, cerebellar, and autonomic systems. Clinical differentiation of MSA from PD may be difficult and leads to misdiagnosis even up to the time of death. Also, dopa sensitivity, as tested with apomorphine or levodopa tests, is not always conclusive.
In MSA, abnormalities on MR images may include not only olivopontocerebellar or putaminal atrophy but also signal intensity abnormalities on T2-weighted images, such as putaminal hypointensity, putaminal slitlike hyperintensity, and pontine cruciform hyperintensity (3,15–18). Findings of a study (19) showed that putaminal hypointense signal changes were more common in patients with MSA than in those with PD when T2*-weighted gradient-echo imaging was used, which indicates that T2*-weighted gradient-echo sequences are of diagnostic value for patients with parkinsonism. Most of these MR imaging abnormalities, however, may also occur in patients with classic signs of PD, thus making the diagnosis of MSA uncertain (3,15–18). Taken together, these data indicate that although neuroimaging can help distinguish MSA from PD, routine MR imaging fails to reliably help discriminate MSA from PD.
Diffusion-weighted imaging is a technique that is commonly used to determine the random movement of water molecules that are aligned with fiber tracts in central nervous system. Pathologic processes that modify tissue integrity can result in an increased apparent diffusion coefficient. Recent evidence demonstrates that diffusion-weighted imaging is able to discriminate between MSA and PD on the basis of putaminal apparent diffusion coefficients, which suggests that this technique may be a useful diagnostic tool for the diagnosis of MSA (20,21).
MR volumetry has also been used to differentiate PD from atypical parkinsonian syndromes such as MSA and progressive supranuclear palsy. Findings of a previous MR-based volumetric study (22) showed a substantial reduction in mean striatal and brainstem volumes in patients with MSA with parkinsonian features compared with patients with PD and control subjects, which suggests that this technique may be helpful in distinguishing between patients with PD and those with MSA. Our study demonstrates that MSA can be easily differentiated from PD when measurement of the MCP width at MR imaging is performed.
In our series, the average width of the MCP was significantly smaller in patients with MSA than in those with PD or in control subjects. This difference was important because the largest MCP width in MSA patients did not reach the smallest MCP width in patients with PD or in control subjects. The measurement of the MCP width on MR images helped discriminate between patients with MSA from those with PD with a sensitivity of 100%, a specificity of 100%, and a positive predictive value of 100%. Indeed, in our series, no patient with PD was classified as having MSA or vice versa when MCP measurements were used.
Our finding of a reduced MCP width in MSA is in agreement with pathologic data showing that pontocerebellar atrophy is the characteristic pathologic change in this disease (10,11). Pontocerebellar fibers originate from pontine gray neurons, which possess axons that cross to the other side of the basilar pons, enter the MCP, and terminate in the cerebellar cortex. The involvement of transverse myelinated pontocerebellar fibers can be seen on routine MR images as a pontine cruciform hyperintensity, a finding typically observed in MSA and in other pathologic conditions that selectively involve the pontocerebellar system (17,23,24).
To evaluate whether the presence of cruciform hyperintensity was associated with a larger MCP atrophy, we separately analyzed MSA patients with and those without cruciform hyperintensity. A significant difference in the average width of MCP was observed between the two groups; patients with cruciform hyperintensity had an MCP width that was significantly smaller than that detected in patients without this MR feature, which confirms that the presence of cruciform hyperintensity was associated with severe atrophy of the MCP. Moreover, disease duration was significantly longer in MSA patients with cruciform hyperintensity than in patients without this MR finding, which suggests that degeneration of pontine transverse fibers increases over time with the progression of the disease.
Although MSA patients with cruciform hyperintensity had a longer disease duration and lower MCP width than did MSA patients without this MR finding, no correlation was found between the average width of MCP and the duration of disease in the whole MSA group. Considering the small number of MSA patients included in our study, we cannot exclude that, in MSA, the degree of MCP atrophy may be related to the severity of the disease. Further studies in a larger sample of MSA patients are needed to better investigate the possible relation between the degree of MCP atrophy on MR images and the progression of the disease.
The major limitation of our study was that it has not been validated with neuropathologic data, and it is possible that the clinical diagnosis may be in error. Indeed, because clinical differentiation of atypical parkinsonian syndromes such as MSA may often be difficult, it could be hypothesized that MSA was misdiagnosed in some patients. However, this does not seem to be our case for the following reasons: (a) Patients included in the study fulfilled the established consensus criteria for a diagnosis of probable MSA; (b) on routine MR images, all subjects had at least one sign suggestive of MSA and eight of 16 patients had cruciform hyperintensity, a finding considered to be highly suggestive of MSA; (c) in all patients, the anteroposterior midbrain diameter was larger than 15.0 mm, a measure rarely observed in progressive supranuclear palsy (25); and (d) measurement of the MCP width allowed correct classification of all patients with MSA included in the study, and no patient was misclassified because all PD patients had MCP widths that were similar to those observed in control subjects.
Our findings indicate that MR imaging can depict MCP atrophy that occurs in MSA and suggest that measurement of MCP width may be useful to help distinguish MSA from PD.
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ADVANCE IN KNOWLEDGE
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- Differentiation of multiple system atrophy (MSA) from Parkinson disease is possible by measuring the middle cerebellar peduncle width on MR images; the width is significantly smaller in patients with MSA than in those with Parkinson disease.
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FOOTNOTES
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Abbreviations: MCP = middle cerebellar peduncle • MSA = multiple system atrophy • PD = Parkinson disease
Authors stated no financial relationship to disclose.
Author contributions: Guarantors of integrity of entire study, G.N., A.Q.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; approval of final version of submitted manuscript, all authors; literature research, G.N., W.A., O.G., P.P., G.A., L.M., P.B., M.Z., A.Q.; clinical studies, G.N., P.P., G.A.; statistical analysis, F.C.; and manuscript editing, G.N., F.F., L.M., P.B., M.Z., A.Q.
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A. Quattrone, G. Nicoletti, D. Messina, F. Fera, F. Condino, P. Pugliese, P. Lanza, P. Barone, L. Morgante, M. Zappia, et al.
MR Imaging Index for Differentiation of Progressive Supranuclear Palsy from Parkinson Disease and the Parkinson Variant of Multiple System Atrophy
Radiology,
December 1, 2007;
246(1):
214 - 221.
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ABSTRACT
INTRODUCTION
