 |
 |

Measurement of the Midbrain Diameter on Routine Magnetic Resonance Imaging
A Simple and Accurate Method of Differentiating Between Parkinson Disease and Progressive Supranuclear Palsy
Monika Warmuth-Metz, MD;
Markus Naumann, MD;
Ilona Csoti, MD;
Laszlo Solymosi, MD
Arch Neurol. 2001;58:1076-1079.
ABSTRACT
 |  |
Anteroposterior diameters of the suprapontine midbrain, the pons, and
the collicular plate were measured in 50 patients with various parkinsonian
syndromes (Parkinson disease [PD] [n = 20], progressive supranuclear palsy
[PSP] [n = 16], and multiple-system atrophy of striatonigral type [n = 14])
and 12 age-matched healthy control subjects by means of axial T2-weighted
magnetic resonance images. While no differences in midbrain diameter were
found between patients with PD (mean, 18.5 mm) and control subjects (mean,
18.2 mm), patients with PSP had significantly lower midbrain diameters (mean,
13.4 mm) than patients with PD and control subjects (P<.001),
without any overlap between these 2 groups. However, midbrain diameters of
patients with multiple-system atrophy were also significantly lower than those
of control subjects and patients with PD, with individual values showing overlap
with the PSP, PD, and control groups. Pontine and collicular plate diameters
did not contribute additional information. We therefore conclude that measurement
of anteroposterior diameter of the midbrain on axial T2-weighted magnetic
resonance images is a reliable means to differentiate patients with PSP from
those with PD and should be incorporated into the diagnostic criteria for
PSP.
INTRODUCTION
Differentiation of Parkinson disease (PD) from atypical parkinsonian
syndromes such as progressive supranuclear palsy (PSP) and multiple-system
atrophy of striatonigral type (MSA-P) on clinical grounds can be inaccurate
at the beginning or even in later stages of the disease.1, 2
Novel imaging techniques, including positron emission tomography,3 single-photon emission computed tomography,4, 5 magnetic resonance (MR) spectroscopy,6, 7 and MR morphometry,4, 5, 8
have improved the accuracy of diagnosis of parkinsonian syndromes on the basis
of abnormalities of basal ganglia or brainstem morphologic characteristics
or receptor density. Magnetic resonance imaging studies in MSA-P have shown
alterations of striatal signal intensity and volume,9, 10
whereas patients with PSP frequently show an atrophy of midbrain structures
that is most pronounced in the superior colliculi of the tegmental plate11, 12, 13, 14, 15, 16
but also of the pons.14, 15, 16
However, the reduction of midbrain diameter as a morphologic hallmark of PSP
has not been analyzed and quantified systematically by contemporary imaging
examinations such as MR imaging. The definition of a distinct cutoff point
between PD and PSP has not yet been provided.
Therefore, the aim of our retrospective study was to evaluate and quantify
the anteroposterior diameters of the pons, the midbrain, and the collicular
plate on routine MR images in various parkinsonian syndromes and healthy age-matched
control subjects to obtain additional neuroimaging criteria for the differentiation
of parkinsonian syndromes.
PATIENTS AND METHODS
Fifty patients with various parkinsonian syndromes and 12 age-matched
healthy volunteers were studied between October 20, 1996, and June 22, 1999.
Twenty patients had typical PD according to the UK Brain Bank Criteria,17 16 patients had PSP (5 possible and 11 probable cases,
2 of which were later confirmed by autopsy) on the basis of National Institute
of Neurological Disorders and Stroke criteria for PSP,18
and 14 patients had MSA-P (4 possible and 10 probable cases) according to
the consensus criteria.19 Mean age, sex, disease
severity according to the Unified Parkinson's Disease Rating Scale (UPDRS;
motor section and global score),20 and disease
duration are given in Table 1.
|
|
|
|
Table 1. Demographic Data in 62 Patients and Control Subjects*
|
|
|
Magnetic resonance imaging was performed according to our routine imaging
protocol on 2 scanners at 1.5-T field strength (Magnetom Vision; Siemens,
Erlangen, Germany; and Gyroscan S15; Philips, Eindhoven, the Netherlands).
Axial conventional T2-weighted spin-echo double-echo sequences with a slice
thickness of 6 or 7 mm were available for every patient. In all except the
patients with PD, additional sagittal T1-weighted MR images with a maximum
slice thickness of 5 mm were available. The maximum midsagittal anteroposterior
diameters of the pons, midbrain, and collicular plate were measured with the
scanners' internal distance measurement device (Figure 1). The evaluation was performed blinded to the individual
diagnosis.
|
|
|
|
Figure 1. Measurement of the midsagittal
anteroposterior diameters of the pons (line 1, A and B), midbrain (line 1,
C and D), and quadrigeminal plate (line 2, A) on sagittal T1- and axial T2-weighted
magnetic resonance images with the imagers' internal distance measurement
device.
|
|
|
For statistical analysis, the Mann-Whitney rank sum test was used to
compare the individual groups. For the evaluation of correlation, the Spearman
rank order test was used. For the evaluation of statistical differences between
multiple groups, the Kruskal-Wallis analysis was used.
RESULTS
MIDBRAIN ATROPHY
There was no difference in midbrain diameters between patients with
PD and control subjects. Patients with PSP showed significantly lower midbrain
diameters than patients with PD and MSA-P and control subjects (P<.001). There was no overlap of midbrain diameters between the
group of patients with PSP and those with PD and control subjects, indicating
that patients with PSP could be distinguished from those with PD and control
subjects on an individual basis (Table 2). However, patients with MSA-P showed overlap of individual diameters
with values from patients with PSP and PD and control subjects (Figure 2).
|
|
|
|
Table 2. Diameters of Midbrain, Pons, and Collicular Plate in 50 Patients
With Parkinsonian Syndromes and 12 Control Subjects*
|
|
|
|
|
|
|
Figure 2. Scatterplot (mean and SD) of the
anteroposterior midbrain diameters for patients with progressive supranuclear
palsy (PSP), multiple-system atrophy of striatonigral type (MSA-P), and Parkinson
disease (PD) and control subjects. The mean values of patients with PSP differ
highly significantly from those of all other patients and controls.
|
|
|
PONTINE ATROPHY
The anteroposterior diameter of the pons measured at its largest distance
perpendicular to the floor of the fourth ventricle (Figure 1) was significantly smaller in the groups of patients with
MSA-P and PSP than in those with PD or control subjects (P<.001), but pontine diameters did not differ significantly between
MSA-P and PSP groups. The pontine diameters did not differ significantly between
patients with PD and control subjects. However, the individual values overlapped
between patients with MSA-P, PSP, and PD and control subjects (Table 2).
ATROPHY OF THE COLLICULAR PLATE
The diameter of the collicular plate was analyzed only in patients with
PSP and MSA-P and control subjects, because in patients with PD, sagittal
MR images were not available. The diameter was lowest in patients with PSP.
There was a small but significant difference between patients with MSA-P and
those with PSP (P = .04) and between patients with
PSP and control subjects (P = .02).
CORRELATION WITH CLINICAL OR DEMOGRAPHIC DATA
In patients with PSP, no statistically significant correlation was found
between reduced midbrain diameters and patients' age (r = -0.19), duration (r = 0.16), or severity
of disease as evaluated by the motor (r = 0.11) and
total (r = 0.21) score of the UPDRS. Patients with
PSP with a mean disease duration of longer than 39.4 months showed nearly
the same mean midbrain diameter (13.5 mm) as did patients with a mean disease
duration of less than 39.4 months (13.2 mm). No significant difference in
midbrain diameters could be demonstrated between more or less severely affected
patients (mean UPDRS motor [30.9] or total [52.7] score).
In 3 patients with PSP, we were able to evaluate a follow-up MR image
after 1 year. Only 1 showed a mild decrease in the midbrain diameter of 1
mm, while the increase in UPDRS rating scale values were nearly identical
in all 3 patients (10 points of average worsening of the total score).
COMMENT
This MR imaging study on brainstem diameters in various parkinsonian
syndromes showed that the simple measurement of the midbrain anteroposterior
diameter may differentiate patients with PSP from those with PD or control
subjects on an individual basis. However, although midbrain diameters were
also significantly reduced in patients with MSA-P, there was overlap with
patients with PSP and PD and control subjects.
Novel imaging techniques such as positron emission tomography, single-photon
emission computed tomography with ligands binding to the nigrostriatal system,
and MR spectroscopy are of additional value to further substantiate the diagnosis
but are not widely accessible.3, 4, 5, 6, 7
Routine imaging techniques are therefore of particular practical value.
Atrophy of the midbrain is one of the typical neuropathologic features
in PSP21, 22 and has already been
described in pneumencephalography and in a few computed tomographic series.12, 14, 16 However, these studies
included only small numbers of patients whose clinical diagnoses were based
on early criteria that might have been less accurate than those currently
proposed for PSP.2
In patients with MSA, degeneration of neurons in the basal ganglia with
resultant signal changes are prominent on autopsy and imaging.9, 10
Most MR imaging studies confirm the diagnostic value of midbrain atrophy
in PSP, but evaluation methods vary widely and include subjective estimation11, 13, 23 or measurement of
the transverse or craniocaudal diameter of the midbrain peduncles.4, 15 Therefore, it is not surprising that,
in addition to reduced midbrain diameters, normal-appearing midbrains have
been reported in PSP.11, 13, 23
A recent report on MSA, PSP, corticobasal degeneration, and healthy controls
confirmed the value of anteroposterior measurement of the midbrain diameter
in PSP.24 However, clinicians endeavor to identify
and differentiate patients with atypical parkinsonian syndromes from those
with typical PD rather than from healthy subjects. Our study, therefore, provides
individual values of midbrain diameters in PD, atypical parkinsonian syndromes
including MSA-P and PSP, and healthy controls from routine MR imaging and
clearly shows that the simple measurement of the midsagittal mesencephalic
anteroposterior diameter on routine MR imaging may differentiate PSP from
typical PD on an individual basis. Anteroposterior midbrain diameters less
than 16 mm strongly argue against the diagnosis of PD, with values less than
14 mm found only in patients with PSP. The observation that midbrain diameters
measured by a neuroradiologist blinded to clinical diagnosis clearly allowed
patients with PSP to be classified as a distinct group without overlap with
PD underlines the value of the National Institute of Neurological Disorders
and Stroke criteria for the clinical diagnosis of PSP. Interestingly, there
was no correlation between duration or severity of PSP and midbrain diameters,
indicating that this measure might also be useful for an early diagnosis of
PSP.
Our study confirmed previous MR imaging findings of occasional brainstem
atrophy in patients with MSA-P.5, 8
In view of the broad overlap between PD and MSA-P values, however, they do
not contribute to the differential diagnosis. The same is true for the pontine
or tegmental plate diameters, whichalthough significantly smaller in
patients with MSA-P and PSP than PDshowed a considerable overlap between
the groups.
In conclusion, the midsagittal mesencephalic diameter measured on standard
routine T2-weighted MR images can be used as a reliable measure to differentiate
between patients with typical PD and those with PSP in vivo. This simple additional
measure should be incorporated in the diagnostic criteria of PSP.
AUTHOR INFORMATION
Accepted for publication January 3, 2001.
This research was performed by the National Parkinson Foundation, Center
of Excellence, Clinical Office, at the Department of Neurology, University
of Würzburg, Würzburg, Germany.
From the Departments of Neuroradiology (Drs Warmuth-Metz and Solymosi)
and Neurology (Drs Naumann and Csoti), University of Würzburg, Würzburg,
Germany.
Corresponding author and reprints: Monika Warmuth-Metz, MD, Department
of Neuroradiology, Josef-Schneider-Str 11, D-97080 Würzburg, Germany
(e-mail: warmuth{at}neuroradiologie.uni-wuerzburg.de).
REFERENCES
 |  |
1. Hughes AJ, Ben-Shlomo Y, Daniel SE, Lees AJ. What features improve the accuracy of clinical diagnosis in Parkinson's
disease: a clinicopathologic study. Neurology. 1992;42:1142-1146.
FREE FULL TEXT
2. Litvan I, Goetz CG, Jankovic J, et al. What is the accuracy of the clinical diagnosis of multiple system atrophy?
a clinicopathologic study. Arch Neurol. 1997;54:937-944.
FREE FULL TEXT
3. Brooks DJ. PET studies on the early and differential diagnosis of Parkinson's
disease. Neurology. 1993;43(suppl 6):S6-S16.
4. Arnold G, Tatsch K, Oertel WH, et al. Clinical progressive supranuclear palsy: differential diagnosis by
IBMZ-SPECT and MRI. J Neural Transm Suppl. 1994;42:111-118.
PUBMED
5. Schulz JB, Klockgether T, Petersen D, et al. Multiple system atrophy: natural history, MRI morphology, and dopamine
receptor imaging with 123IBZM-SPECT. J Neurol Neurosurg Psychiatry. 1994;57:1047-1056.
FREE FULL TEXT
6. Davie CA, Wenning GK, Barker GJ, et al. Differentiation of multiple system atrophy from idiopathic Parkinson's
disease using proton magnetic resonance spectroscopy. Ann Neurol. 1995;37:204-210.
FULL TEXT
|
ISI
| PUBMED
7. Tedeschi G, Litvan I, Bonavita S, et al. Proton magnetic resonance spectroscopic imaging in progressive supranuclear
palsy, Parkinson's disease and corticobasal degeneration. Brain. 1997;120:1541-1552.
FREE FULL TEXT
8. Albanese A, Colosimo C, Bentivoglio AR, et al. Multiple system atrophy presenting as parkinsonism: clinical features
and diagnostic criteria. J Neurol Neurosurg Psychiatry. 1995;59:144-151.
FREE FULL TEXT
9. Kraft E, Schwarz J, Trenkwalder C, Vogl T, Pfluger T, Oertel WH. The combination of hypointense and hyperintense signal changes on T2-weighted
magnetic resonance imaging sequences: a specific marker of multiple system
atrophy? Arch Neurol. 1999;56:225-228.
FREE FULL TEXT
10. Konagaya M, Sakai M, Matsuoka Y, Goto Y, Yoshida M, Hashizume Y. Pathological correlate of slitlike changes on MRI at the putaminal
margin in multiple system atrophy. J Neurol. 1999;246:142-143.
FULL TEXT
|
ISI
| PUBMED
11. Savoiardo M, Girotti F, Strada L, Ciceri E. Magnetic resonance imaging in progressive supranuclear palsy and other
parkinsonian disorders. J Neural Transm Suppl. 1994;42:93-110.
PUBMED
12. Haldeman S, Goldman JW, Hyde J, Pribram HFW. Progressive supranuclear palsy, computed tomography and response to
antiparkinsonian drugs. Neurology. 1981;31:442-445.
FREE FULL TEXT
13. Savoiardo M, Strada L, Girotti F, et al. MR imaging in progressive supranuclear palsy and Shy-Drager syndrome. J Comput Assist Tomogr. 1989;13:555-560.
ISI
| PUBMED
14. Masucci EF, Borts FT, Smirniotopoulos JG, Kurtzke JF, Schellinger D. Thin section CT of midbrain abnormalities in progressive supranuclear
palsy. AJNR Am J Neuroradiol. 1985;6:767-772.
ABSTRACT
15. Masucci EF, Borts FT, Perl SM, Wener L, Schwankhaus J, Kurtzke JF. MR vs CT in progressive supranuclear palsy. Comput Med Imag Graph. 1995;19:361-368.
FULL TEXT
|
ISI
| PUBMED
16. Schonfeld SM, Globe LI, Sage JI, Safer JN, Duvoisin RC. Computed tomographic findings in progressive supranuclear palsy: correlation
with clinical grade. Mov Disord. 1987;2:263-278.
FULL TEXT
|
ISI
| PUBMED
17. Calne DB, Snow BJ, Lee C. Criteria for diagnosing Parkinson's disease. Ann Neurol. 1992;32(suppl):S125-S127.
18. Litvan I, Agid Y, Calne D, et al. Clinical research criteria for the diagnosis of progressive supranuclear
palsy (Steele-Richardson-Olszewski syndrome): report of the NINDS-SPSP International
Workshop. Neurology. 1996;47:1-9.
FREE FULL TEXT
19. Gilman S, Low PA, Quinn N, et al. Consensus statement on the clinical diagnosis of multiple system atrophy. J Neurol Sci. 1999;163:94-98.
FULL TEXT
|
ISI
| PUBMED
20. Fahn S, Elton RL members of the UPDRS Development Committee. Unified Parkinson's Disease Rating Scale. In: Fahn S, Marsden CD, Goldstein M, et al, eds. Recent Developments in Parkinson's Disease. New York, NY: Macmillan
Publishing Co; 1987:153-163.
21. Yagishita A, Oda M. Progressive supranuclear palsy: MRI and pathological findings. Neuroradiology. 1996;38(suppl):S60-S66.
22. Aiba I, Hashizume Y, Yoshida M, Okuda S, Murakami N, Ujihira N. Relationship between brainstem MRI and pathologic findings in progressive
supranuclear palsy: study in autopsy cases. J Neurol Sci. 1997;152:210-217.
FULL TEXT
|
ISI
| PUBMED
23. Soliveri P, Monza D, Radice D, et al. Cognitive and magnetic resonance imaging aspects of corticobasal degeneration
and progressive supranuclear palsy. Neurology. 1999;53:502-507.
FREE FULL TEXT
24. Schrag A, Good CD, Miszkiel K. Differentiation of atypical parkinsonian syndromes with routine MRI. Neurology. 2000;54:697-702.
FREE FULL TEXT
CiteULike Connotea Del.icio.us Digg Reddit Technorati Twitter
What's this?
RELATED ARTICLE
Archives of Neurology Reader's Choice: Continuing Medical Education
Arch Neurol. 2001;58(7):1172-1174.
FULL TEXT
THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES
 |
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
| FULL TEXT
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.
ABSTRACT
| FULL TEXT
Is it Parkinson's disease, and if not, what is it?
Taylor and Counsell
PN 2006;6:154-165.
FULL TEXT
MR Imaging of Middle Cerebellar Peduncle Width: Differentiation of Multiple System Atrophy from Parkinson Disease.
Nicoletti et al.
Radiology 2006;239:825-830.
ABSTRACT
| FULL TEXT
Diffusion tensor imaging and voxel based morphometry study in early progressive supranuclear palsy
Padovani et al.
J. Neurol. Neurosurg. Psychiatry 2006;77:457-463.
ABSTRACT
| FULL TEXT
Penguins and hummingbirds: Midbrain atrophy in progressive supranuclear palsy
Groschel et al.
Neurology 2006;66:949-950.
FULL TEXT
Infratentorial Abnormalities in Vascular Dementia
Bastos Leite et al.
Stroke 2006;37:105-110.
ABSTRACT
| FULL TEXT
New and reliable MRI diagnosis for progressive supranuclear palsy
Oba et al.
Neurology 2005;64:2050-2055.
ABSTRACT
| FULL TEXT
Parkinson disease, brain volumes, and subthalamic nucleus stimulation
Bonneville et al.
Neurology 2005;64:1598-1604.
ABSTRACT
| FULL TEXT
Radiologic evidence for absence of the facial nerve in Mobius syndrome
Verzijl et al.
Neurology 2005;64:849-855.
ABSTRACT
| FULL TEXT
Quantitative MRI measurement of superior cerebellar peduncle in progressive supranuclear palsy
Paviour et al.
Neurology 2005;64:675-679.
ABSTRACT
| FULL TEXT
Pathological substrate for regional distribution of increased atrophy rates in progressive supranuclear palsy
Paviour et al.
J. Neurol. Neurosurg. Psychiatry 2004;75:1772-1775.
ABSTRACT
| FULL TEXT
MR Imaging of the Superior Profile of the Midbrain: Differential Diagnosis between Progressive Supranuclear Palsy and Parkinson Disease
Righini et al.
Am. J. Neuroradiol. 2004;25:927-932.
ABSTRACT
| FULL TEXT
Voxel based morphometry reveals a distinct pattern of frontal atrophy in progressive supranuclear palsy
Brenneis et al.
J. Neurol. Neurosurg. Psychiatry 2004;75:246-249.
ABSTRACT
| FULL TEXT
|