Vous êtes sur la page 1sur 8

The Role of Imaging

in the Diagnosis
of Vascular Parkinsonism
Jan C.M. Zijlmans, MD, PhD

 Vascular parkinsonism  MRI  CT  SPECT  Diagnosis

PARKINSONISM preserved than in patients with Parkinson disease

Parkinsonism is a syndrome that features Depending on their onset, 2 types of VP can be
bradykinesia (slowness of the initiation of voluntary distinguished6: one with an insidious onset and its
movement) and at least 1 of the following condi- vascular lesions diffusely located in the watershed
tions: rest tremor, muscular rigidity, or postural areas (VPi) and the other with an acute onset and
instability. In 1929, Critchley1 identified a type of lesions located in the subcortical gray nuclei
parkinsonism caused by cerebrovascular disease (striatum, globus pallidus, and thalamus) (VPa).
in his report on ‘‘arteriosclerotic parkinsonism.’’ It Winikates and Jankovic8 later confirmed the
required the development of computed 2 different types of onset. In about one-quarter of
tomography (CT) and magnetic resonance the patients with VP, the symptoms start
imaging (MRI) 50 years later to find evidence for acutely.6,8
Critchley’s ideas and what is now commonly
known as vascular parkinsonism (VP).2–6 Ischemic
vascular lesions that may lead to VP are lacunar CLINICAL DIAGNOSIS
infarctions, white matter hyperintensities, and
less common large vessel infarctions. A compar- Winikates and Jankovic8 categorized patients with
ison of 5 different European studies showed parkinsonism and a vascular score of 2 or more on
a prevalence rate of 3% of VP.7 In case the onset a rating scale as having VP. In this way, many
of parkinsonism was associated with a cerebro- patients with PD and vascular risk factors can be
vascular event, VP was diagnosed. Probably the misdiagnosed as having VP. Criteria for the clinical
real prevalence is higher because only few diagnosis of VP have been proposed, which are
patients with VP have an acute onset.6,8 derived from a postmortem examination study.10
See Box 1 for the criteria for clinical diagnosis of

In the classical type of VP, as reported by Thomp-
son and Marsden4 and FitzGerald and Jankovic,5 In the ‘‘classical clinical type’’ of VP, parkinsonism
difficulty in walking is the most important initial is attributed to diffuse periventricular and frontal
symptom. Therefore, the classical type is also white matter damage4 because similar clinical
called lower-half4 or lower-body parkinsonism.5 features occur in normal pressure hydrocephalus
In patients suffering from the classical type, the and in some cases of frontal parasagittal menin-

gait is disordered by shuffling, short steps, variable gioma, in which the same structures are compro-
base (narrow to wide), start and turn hesitation, mised. According to Thompson and Marsden,4
and moderate disequilibrium. In addition, the arm disconnection of thalamocortical fibers to the
swing in patients with VP is usually more supplementary motor area and cerebellar fibers

Department of Neurology, Amphia Hospital, Molengracht 21, 4818 CK, Breda, The Netherlands
E-mail address: jzijlmans@amphia.nl

Neuroimag Clin N Am 20 (2010) 69–76

1052-5149/09/$ – see front matter ª 2010 Elsevier Inc. All rights reserved.
70 Zijlmans

Box 1 thalamocortical drive to premotor areas and also

Criteria for the clinical diagnosis of probableVP subsequent development of parkinsonism. Ac-
cording to many previous publications, parkin-
a. Parkinsonism sonism is also attributed to strategic infarcts in
bradykinesia (slowness of initiation of the basal ganglia or thalamus. A causal relation-
voluntary movement with progressive reduc- ship between strategic infarcts and parkinsonism
tion in speed and amplitude of repetitive is reported only in a few publications that
actions in either upper limb or lower limb, described the cases in which the onset is (sub)
including the presence of reduced step acute or accompanied by other symptoms of
length) and at least 1 of the following: a stroke related to the same lesion.2,3,6,8,12–24
rest tremor, muscular rigidity, or postural Lesions in specific areas that theoretically can
instability not caused by primary visual, cause parkinsonism (GPe, VL/VA of thalamus,
vestibular, cerebellar or proprioceptive and SNc) have been described by a few investi-
dysfunction gators.2,16,18,21–23 The infarct is located in the
b. Cerebrovascular disease hemisphere or brainstem contralateral to parkin-
sonism in most cases in which a vascular cause
 evidence of relevant cerebrovascular
disease by brain imaging (CT or MRI) or is acceptable and a single lesion is seen in the
 the presence of focal signs or symptoms basal ganglia or thalamus.12,14–18,20–22,24
that are consistent with stroke.
c. A relationship between these 2 disorders. In PATHOPHYSIOLOGY
The most supported hypothesis about the
 an acute or delayed progressive onset with pathogenesis of subcortical lesions was originally
infarcts in or near areas that can increase proposed by Binswanger and Alzheimer.25,26
the basal ganglia motor output (GPe They suggested that the white matter softening
[globus pallidus pars externa] or SNc [sub-
can be attributed to subcortical ischemia as
stantia nigra pars compacta]) or decrease
the thalamocortical drive directly (VL[ven- a result of arteriolosclerosis of the long penetrating
tral lateral] nuclei of the thalamus, large arteries. According to this view, arteriolosclerosis
frontal lobe infarct). At onset, parkin- of long penetrating arteries that are poorly
sonism consists of a contralateral bradyki- provided with collateral anastomoses can result
netic rigid syndrome or shuffling gait in ischemia of the distal fields of these vessels,
within 1 year after a stroke (VPa). that is, periventricularly and in the watershed
 an insidious onset of parkinsonism with zones. Transient episodes of hypotension caused
extensive subcortical white matter lesions, by excessive antihypertensive medication or heart
bilateral symptoms at onset, and the failure27 and hyperviscosity28 may provoke or
presence of early shuffling gait or early
aggravate white matter disease in an already
cognitive dysfunction (VPi); the ‘‘classical
clinical type.’’ compromised cerebral blood flow.29,30 The typi-
cally hypertensive changes of small vessel disease
Exclusion criteria can occasionally be found in a patient who is not
 a history of repeated head injury hypertensive or diabetic.31 Conversely, not every
 encephalitis elderly patient with hypertension develops small
 neuroleptic treatment at onset of symptoms vessel disease.32 These points suggest that
 the presence of cerebral tumor or communi- factors other than hypertension and diabetes,
cating hydrocephalus such as a cerebrovascular accident, cardiac
 other alternative explanation for Parkinson
disease, or carotid pathology, are probably also
involved in the development of hypertensive arte-
riolopathy.33 Many investigators stated that the
clinical significance of subcortical lesions depends
to the leg area is the underlying mechanism that on the severity and location of lesions.6,32,34
causes the gait disorder in VP. A threshold extent of subcortical lesions may be
In accordance with current concepts of puta- necessary before symptoms appear.6,34,35
menal efferents directed toward the basal ganglia
output nuclei,11 one might expect that vascular DIFFERENTIAL DIAGNOSIS
lesions in the SNc (substantia nigra pars
compacta), GPe (globus pallidus pars externa), Features that are usually considered to favor
or the VA (ventral anterior)/VL (ventral lateral) a diagnosis of idiopathic PD36 are also frequently
nuclei of the thalamus induce decreased present in VP and include micrographia,
Role of Imaging in Vascular Parkinsonism Diagnosis 71

cogwheeling, stooped posture, facial masking, thalamus, substantia nigra, and frontal lobe). MRI
hypophonia, and a positive response to levodopa. is preferred to demonstrate the presence of
However, application of the more stringent UK strategic vascular lesions because of its greater
Parkinson’s Disease Society Brain Bank criteria capabilities to show small lesions in regions that
for the diagnosis of idiopathic PD37 excludes this are difficult to image with CT, such as the globus
diagnosis in most patients with VP. In case a slowly pallidus, thalamus, and substantia nigra, and also
progressive gait disorder presents itself with because of the possibility to scan in different direc-
a shuffling gait, then a normal pressure tions (eg, coronal and sagittal). The different
hydrocephalus or a frontal lobe tumor must be T1- and T2-weighted sequences have their own
considered. A clinical diagnosis together with qualities, and when combined, they give compli-
a radiologic diagnosis of probable multiple system mentary information on the characteristics and
atrophy,38 progressive supranuclear palsy probable cause of ischemic pathology. This may
(PSP),39 or dementia with Lewy bodies40 probably be important to fulfill the diagnostic criteria
excludes a diagnosis of VP in most cases.10 mentioned earlier. T1-weighted images reveal la-
Dubinsky and Jankovic41 and Winikates and Jan- cunes and frontal cortical infarcts. Fluid attenuated
kovic42 suggested the presence of a particular inversion recovery (FLAIR) is best suited for the
subtype of VP that they called vascular PSP. In assessment of white matter lesions. It has the
one report, the brains of 2 patients with vascular advantage of suppressing cerebrospinal fluid
PSP showed (besides the common diffuse white signal, allowing a simple distinction of lacunes
matter lesions) additional lesions in the dorsal and perivascular spaces from ischemic white
pons and in the thalamus. matter lesions, both of which are bright on
standard T2-(T)SE weighted images.43,44 For the
assessment of ischemic lesions in the thalamus
Brain Imaging
and infratentorial regions, conventional T2-weighted
In the last century, CT and MRI were mainly used images are preferred.45 In addition, T2*-weighted
to exclude hydrocephalus, mass lesions, or gradient echo sequences are more sensitive for
subdural hematomas in atypical parkinsonism. the detection of hemorrhagic lacunae than spin
They now can support the clinical diagnosis of echo and FLAIR sequences.46–49 An imaging
VP with positive imaging findings. One has to protocol using T1, T2, T2*, and FLAIR images
consider the 2 different locations of lesions with may therefore optimize diagnostic capabilities of
their related types of onset: an insidious onset MRI for VP (Table 1). Fig. 1 and 2 show MRI scans
type presenting itself with white matter lesions in patients with VP with an insidious and an acute
that are diffusely located in the watershed areas onset.
and an acute onset type with lesions located in Because subcortical lesions in the basal ganglia
contralateral strategic areas (globus pallidus, and the white matter can also occur in older

Table 1
Example of imaging protocol for the detection of cerebral vascular lesions

Coronal 3D T1 gradient echo TR 15 ms

TE 7 ms
T1 500 ms
Slice thickness 1 mm
Flip angle 15 –30
Axial T2 spin echo TR 4000 ms
TE 100 ms
Slice thickness 3–5 mm
Axial or coronal FLAIR TR 8000 ms
TE 102 ms
T1 2000 ms
Slice thickness 3–5 mm
Axial T2* gradient echo TR 650 ms
TE 15 ms
Slice thickness 3–5 mm
Flip angle R20

Abbreviations: T1, inversion time; TE, echo time; TR, repetition time.
72 Zijlmans

Fig. 1. Axial T2-weighted spin echo (A) and coronal FLAIR (B) MRI scan of a 67-year-old patient with VPi with
a slowly, progressive frontal gait disorder showing vascular lesions diffusely in the white matter.

people without parkinsonism,50,51 one has to in 10% to 30% of asymptomatic elderly patients
relate not only the severity but also the location having vascular risk factors.51,52 Vascular lesion
of lesions with clinical features. Partially or widely load may serve as a marker of disease severity.
confluent subcortical lesions have been reported Different methods can be used for the

Fig. 2. (A) Axial T2-weighted MRI scan of an 80-year-old patient with VP showing lacunar infarctions involving the
globus pallidus on both sides. Two years earlier, the patient noticed a shuffling gait and bradykinesia on both
sides immediately after resuscitation. (B) DAT SPECT of the patient showing striatal FP-CIT uptake reduction in
a similar distribution as in PD, only less asymmetrical.
Role of Imaging in Vascular Parkinsonism Diagnosis 73

measurement of ischemic white matter lesions, [99m-Tc] TRODAT) and are therefore useful in
ranging from visual rating to fully computerized showing a reduction of presynaptic tracer uptake,
techniques. Visual rating of ischemic white matter which correlates with disease duration and
lesions is quick, and several scales are available severity of PD.57
with good reproducibility.53 However, the visual A significant presynaptic dopaminergic deficit
scales often do not provide information about can be found in VPi and VPa groups when
size and location and are usually not linear. compared with normal controls.21,58–63 The dopa-
Furthermore, scores from different visual rating minergic deficit in patients with VP that was
scales are not directly comparable.54 They display demonstrated by [123I] FP-CIT SPECT (single-
ceiling effects and poor discrimination of absolute photon emission computed tomography) is as
volumes. Consequently, they may be less sensi- marked as in PD, and it also affects the striatum
tive than volumetric studies in differentiating clin- in a pattern similar to that described in PD,58 in
ical groups.55 Volumetric studies mainly use which (in accordance with neuropathologic
semiautomated methods that may provide evidence of selective degeneration of nigrostriatal
detailed information on location and size, but neurons)64 a predominant reduction of tracer
they are time consuming.56 Further work is needed uptake is typically seen in the posterior putamen.65
to make automated lesion counting more easy. In patients with VP, the dopaminergic deficit is re-
The differential diagnosis of multifocal or diffuse flected in the caudate/putamen radioactivity
cerebral demyelinization in adults is shown in ratios, similar to the PD group, which were signifi-
Box 2. cantly higher than in normal controls. Patients with
VPi, show a presynaptic dopaminergic deficit
Dopamine Transporter Single-photon similar to patients with VPa. Normal presynaptic
Emission Computed Tomography Scan tracer binding may also be found in patients with
VP,66–68 showing that VP is heterogeneous in its
A series of cocaine analogs have been developed etiology. See Fig. 2B for DAT SPECT in VP.
successfully for imaging dopamine transporters To distinguish VP from PD, the presence of
(DATs) (eg, [123I] b-CIT, [123I]-FP-CIT, and a symmetric FP-CIT uptake in the basal ganglia
may help.58 Asymmetry of degeneration of nigros-
triatal dopaminergic projections to the motor stria-
Box 2 tum is a hallmark of PD that underlies the common
Causes of multifocal or diffuse cerebral initial asymmetry of clinical features at presenta-
demyelinization in adults, besides small vessel tion. The mean asymmetry index that compares
disease. right to left striatal FP-CIT binding in most patients
Alzheimer disease with VP, however, is normal and lower than in
PD.58 This is consistent with the idea that the
Multiple sclerosis
disease in the vascular group usually is more
Progressive multifocal leukoencephalopathy diffusely distributed than in PD, and the parkin-
Human immunodeficiency virus encephalopathy sonism is relatively symmetric in most of the
Creutzfeldt-Jakob disease patients.10 The presence of MRI evidence of
diffuse small vessel disease, in most patients,
Hyperperfusion syndrome
may explain this observation. Only occasionally
Posttransfusion syndrome the clinical presentation of VP at onset may be
Proximal myotonic myopathy asymmetrical, especially when the disease onset
is acute and SPECT is performed in the acute
phase. Substantial asymmetry of presynaptic
Radiotherapy uptake reduction in patients with VP may therefore
Chemotherapy be a less common finding.21,59–63
Postinfectious demyelinization Some patients with VPa may show a ‘‘punched
out’’ FP-CIT uptake in the putamen or globus
Posthypoxic ischemic encephalopathy
pallidus, corresponding to a focal infarc-
Cyclosporin or other immunosuppressants tion.58,61–63
Vitamin B12 deficiency
a-Galactosidase deficiency (Fabry disease) SUMMARY
Data from Van Gijn J. Leukoaraiosis and vascular Criteria for the clinical diagnosis of VP have been
dementia. Neurology 1998;51(Suppl 3):S3–8.
proposed, which are derived from a postmortem
examination study. CT and MRI can support this
74 Zijlmans

clinical diagnosis with positive imaging findings. syndrome]. Rev Neurol (Paris) 1993;149:565–7 [in
One has to consider the 2 different types of onset French].
with their related locations of lesions: an insidious 15. Lee MS, Lee SA, Heo JH, et al. A patient with
onset type presenting itself with white matter a resting tremor and a lacunar infarction at the
lesions diffusely located in the watershed areas border between the thalamus and the internal
and an acute onset type with lesions located in capsule. Mov Disord 1993;8:244–6.
contralateral strategic areas. DAT SPECT may 16. De La Fuente Fernandez R, Lopez J, Rey del
also be of help to distinguish VP from PD and other Corral P, et al. Peduncular hallucinosis and right
parkinsonisms. hemiparkinsonism caused by left mesencephalic
infarction. J Neurol Neurosurg Psychiatr 1994;57:
17. Pullicino P, Lichter D, Benedict R. Micrographia with
I would like to thank Dr Th. De Jong, radiologist, of cognitive dysfunction: ‘‘minimal’’ sequelae of a puta-
my hospital for advising me. minal infarct. Mov Disord 1994;9:371–3.
18. Kulisevsky J, Avila A. Bipolar affective disorder and
REFERENCES unilateral parkinsonism after a brainstem infarction.
Mov Disord 1995;10:799–801.
1. Critchley M. Arteriosclerotic parkinsonism. Brain 19. Mark MH, Sage JI, Walters AS, et al. Binswanger’s
1929;52:23–83. disease presenting as levodopa-responsive parkin-
2. Tolosa ES, Santamaria J. Parkinsonism and basal sonism: clinicopathological study of three cases.
ganglia infarcts. Neurology 1984;34:1516–8. Mov Disord 1995;10:450–4.
3. Friedman A, Kang UJ, Tatemichi TK, et al. A case of 20. Reider-Grosswasser I, Bornstein N, Korczyn A.
parkinsonism following striatal lacunar infarction. Parkinsonism in patients with lacunar infarcts of the
J Neurol Neurosurg Psychiatr 1986;49:1087–8. basal ganglia. Eur Neurol 1995;35:46–9.
4. Thompson PD, Marsden CD. Gait disorder of 21. Boecker H, Weindl A, Leenders K, et al. Secondary
subcortical arteriosclerotic encephalopathy: Bins- parkinsonism due to focal substantia nigra lesions:
wanger’s disease. Mov Disord 1987;2:1–8. a PET study with [18F] FDG and [18F] fluorodopa.
5. FitzGerald PM, Jankovic J. Lower body parkin- Acta Neurol Scand 1996;93:387–92.
sonism: evidence for vascular etiology. Mov Disord 22. Fénelon G, Houéto J. Unilateral parkinsonism
1989;4:249–60. following a large infarct in the territory of the lenticu-
6. Zijlmans JC, Thijssen HO, Vogels OJ, et al. MRI in lostriate arteries. Mov Disord 1997;12:1086–90.
patients suspected of vascular parkinsonism. 23. Leduc V, Montagne B, Destée A. Parkinsonism
Neurology 1995;45:2183–8. consecutive to an hemorrhagic lesion of the sub-
7. de Rijk M, Tzourio C, Breteler M, et al. Prevalence of stantia nigra. Mov Disord 1997;12(Suppl 1):2.
parkinsonism and Parkinson’s disease in Europe: the 24. Alarcón F, Zijlmans JCM, Dueñas G, et al. Post-
EURPARKINSON collaborative study. J Neurol Neu- stroke movement disorders: report of 56 patients.
rosurg Psychiatr 1997;62:10–5. J Neurol Neurosurg Psychiatr 2004;75:1568–74.
8. Winikates J, Jankovic J. Clinical correlates of 25. Alzheimer A. Die Seelenstörung auf arteriosclero-
vascular parkinsonism. Arch Neurol 1999;56: tischer Grundlage. [Psychiatric disturbance with
98–102. arteriosclerotic basis]. Z Psychiat 1902;59:695–711
9. Zijlmans JC, Poels PJ, Duysens J, et al. Quantitative [in German].
gait analysis in patients with vascular parkinsonism. 26. Blass JP, Hoher S, Nitsch R. A translation of Otto
Mov Disord 1996;11(5):501–8. Binswanger’s article, ‘the delineation of the general-
10. Zijlmans J, Daniel S, Hughes A, et al. A clinico-path- ized progressive paralyses’. Arch Neurol 1991;48:
ological investigation of vascular parkinsonism (VP). 961–72.
Including clinical criteria for the diagnosis of VP. Mov 27. Breteler MM, van Amerongen NM, van Swieten JC,
Disord 2004;19:630–40. et al. Cognitive correlates of ventricular enlargement
11. DeLong MR, Wichmann T. Circuits and circuit disor- and cerebral white matter lesions on magnetic reso-
ders of the basal ganglia. Arch Neurol 2007;64(1): nance imaging. The Rotterdam study. Stroke 1994;
20–4. 25:1109–15.
12. Chang CM, Yu YL, Leung SY, et al. Vascular pseudo- 28. Schneider R, Ringelstein EB, Zeumer H, et al. The
parkinsonism. Acta Neurol Scand 1992;86:588–92. role of plasma hyperviscosity in subcortical arterio-
13. Mayo J, Arias M, Leno C, et al. Vascular parkin- sclerotic encephalopathy (Binswanger’s disease).
sonism and periarteritis nodosa. Neurology 1986; J Neurol 1987;234:67–73.
36:874–5. 29. Caplan LR, Schoene WC. Clinical features of
14. Tison F, Duché B, Loiseau P. Syndrome hemiparkin- subcortical arteriosclerotic encephalopathy (Bins-
sonien vasculaire. [Vascular hemiparkinson wanger’s disease). Neurology 1978;28:1206–15.
Role of Imaging in Vascular Parkinsonism Diagnosis 75

30. Thomas D, du Boulay G, Marshall J, et al. Effect of 45. Bastos Leite AJ, van Straaten EC, Scheltens P, et al.
hematocrit on cerebral blood flow in man. Lancet Thalamic lesions in vascular dementia: low sensi-
1977;2:941–3. tivity of fluid-attenuated inversion recovery (FLAIR)
31. Ma K, Lundberg P, Lilja A, et al. Binswanger’s imaging. Stroke 2004;35(2):415–9.
disease in the absence of chronic arterial hyperten- 46. Challa VR, Moody DM. The value of magnetic reso-
sion: a case report with clinical, radiological and nance imaging in the detection of type II hemor-
immunohistochemical observations on intracerebral rhagic lacunes. Stroke 1989;20(6):822–5.
blood vessels. Acta Neuropathol 1992;83:434–9. 47. Fazekas F, Kleinert R, Roob G, et al. Histopathologic
32. van Swieten JC, Geyskes GG, Derix MM, et al. analysis of foci of signal loss on gradient-echo T2*-
Hypertension in the elderly is associated with white weighted MR images in patients with spontaneous
matter lesions and cognitive decline. Ann Neurol intracerebral hemorrhage: evidence of microangiop-
1991;30:825–30. athy-related microbleeds. AJNR Am J Neuroradiol
33. Van Gijn J. Leukoaraiosis and vascular dementia. 1999;20(4):637–42.
Neurology 1998;51(Suppl 3):S3–8. 48. Kim DE, Bae HJ, Kim H, et al. Gradient echo
34. Rao SM, Mittenberg W, Bernardin L, et al. Neuropsy- magnetic resonance imaging in the prediction of
chological test findings in subjects with leukoaraio- hemorrhagic vs ischemic stroke: a need for the
sis. Arch Neurol 1989;46:40–4. consideration of the extent of leukoariosis. Arch
35. Boone KB, Miller BL, Lesser IM, et al. Neuropsycho- Neurol 2002;59(3):425–9.
logical correlates of white matter lesions in healthy 49. Ripoll MA, Sjösteen B, Hartman M, et al. MR
elderly subjects. Arch Neurol 1992;49:549–54. detectability and appearance of small experi-
36. Jankovic J. Clinical aspects of Parkinson’s disease. mental intracranial hematomas at 1.5 T and
In: Marsden CD, Fahn S, editors. The assessment 0.5 T. A 6-7-month follow-up study. Acta Radiol
and therapy of parkinsonism (New trends in clinical 2003;44(2):199–205.
neurology series). New Jersey (NJ): Parthenon 50. Fisher CM. Lacunes: small, deep cerebral infarcts.
Publishing Group; 1990. p. 53–75. Neurology 1965;15:774–84.
37. Hughes AJ, Daniel SE, Kilford L, et al. Accuracy of 51. Awad IA, Spetzler RF, Hodak JA, et al. Incidental
clinical diagnosis of idiopathic Parkinson’s disease: subcortical lesions identified on magnetic reso-
a clinico-pathological study of 100 cases. J Neurol nance imaging in the elderly. 1. Correlation with
Neurosurg Psychiatr 1992;55:181–4. age and cerebrovascular risk factors. Stroke 1986;
38. Gilman S, Low P, Quinn N, et al. Consensus state- 17:1084–9.
ment on the diagnosis of multiple system atrophy. 52. Fazekas F. Magnetic resonance signal abnormalities
J Neurol Sci 1999;163:94–8. in asymptomatic individuals: their incidence and
39. Litvan I, Agid Y, Calne D, et al. Clinical research functional correlates. Eur Neurol 1989;29:164–8.
criteria for the diagnosis of progressive supranuclear 53. Scheltens P, Erkinjunti T, Leys D, et al. White matter
palsy (Steele-Richardson-Olszewski syndrome): changes on CT and MRI: an overview of visual rating
report of the NINDS-SPSP International Workshop. scales. European Task Force on Age-Related White
Neurology 1996;47:1–9. Matter Changes. Eur Neurol 1998;39(2):80–9.
40. McKeith IG, Galasko D, Kosaka K, et al. Consensus 54. Pantoni L, Simoni M, Pracucci G, et al. Visual rating
guidelines for the clinical and pathologic diagnosis scales for age-related white matter changes (leu-
of dementia with Lewy bodies (DLB): report of the koaraiosis): can the heterogeneity be reduced?
consortium on DLB international workshop. Stroke 2002;33(12):2827–33.
Neurology 1996 Nov;47(5):1113–24 [review]. 55. van Straaten EC, Fazekas F, Rostrup E, et al. Impact
41. Dubinsky RM, Jankovic J. Progressive supranuclear of white matter hyperintensities scoring method on
palsy and a multi-infarct state. Neurology 1987;37: correlations with clinical data: the LADIS study.
570–6. Stroke 2006;37(3):836–40.
42. Winikates J, Jankovic J. Vascular progressive supra- 56. Anbeek P, Vincken KL, van Bochove GS, et al. Prob-
nuclear palsy. J Neural Transm Suppl 1994;42: abilistic segmentation of brain tissue in MR imaging.
189–201. Neuroimage 2005;27(4):795–804.
43. Haynal JV, Bryant DJ, Kasuboski L, et al. Use of fluid 57. Booij J, Tissingh G, Winogrodzka A, et al. Imaging of
attenuated inversion recovery (FLAIR) pulse the dopaminergic neurotransmission system using
sequences in MRI of the brain. J Comput Assist single-photon emission tomography and positron
Tomogr 1992;16(6):841–4. emission tomography in patients with parkinsonism.
44. De Coene B, Haynal JV, Gatehouse P, et al. MR of Eur J Nucl Med 1999;26(2):171–82.
the brain using fluid-attenuated inversion recovery 58. Zijlmans J, Evans A, Fontes F, et al. [123I] FP-CIT
(FLAIR) pulse sequences. AJNR Am J Neuroradiol SPECT study of vascular parkinsonism and Parkin-
1992;13(6):1555–64. son’s disease. Mov Disord 2007;22(9):1278–85.
76 Zijlmans

59. Peters S, Eising EG, Przuntek H, et al. Vascular 65. Loberboym M, Djaldetti R, Melamed E, et al. 123I-
parkinsonism: a case report and review of the litera- FP-CIT SPECT imaging of dopamine transporters
ture. J Clin Neurosci 2001;8(3):268–71. in patients with cerebrovascular disease and clinical
60. Remy P, de Recondo A, Defer G, et al. Peduncular diagnosis of vascular parkinsonism. J Nucl Med
‘rubral’ tremor and dopaminergic denervation: 2004;45(10):1688–93.
a PET study. Neurology 1995;45:472–7. 66. Brooks DJ, Ibanez V, Sawle GV, et al. Differing
61. Marshall V, Grosset D. Role of dopamine transporter patterns of striatal 18F-dopa uptake in Parkinson’s
imaging in routine clinical practice. Mov Disord disease, multiple system atrophy, and progressive
2003;18(12):1415–23. supranuclear palsy. Ann Neurol 1990;28(4):
62. Peralta C, Werner P, Holl B, et al. Parkinsonism 547–55.
following striatal infarcts: incidence in a prospective 67. Tzen KY, Lu CS, Yen TC, et al. Differential diagnosis
stroke unit cohort. J Neural Transm 2004;111:1473–83. of Parkinson’s disease and vascular parkinsonism
63. Plotkin M, Amthauer H, Quill S, et al. Imaging of dopamine by (99m)Tc-TRODAT-1. J Nucl Med 2001;42(3):
transporters and D2 receptors in vascular parkinsonism: 408–13.
a report of four cases. J Neural Transm 2005;112:1355–61. 68. Gerschlager W, Bencsits G, Pirker W, et al.
64. Fearnley JM, Lees AJ. Aging and Parkinson’s [123I]beta-CIT SPECT distinguishes vascular parkin-
disease: substantia nigra regional selectivity. Brain sonism from Parkinson’s disease. Mov Disord 2002;
1991;114:2283–301. 17(3):518–23.