- Email: [email protected]
Movement disorders and Creutzfeldt-Jakob disease: A review
Parkinsonism and Related Disorders 12 (2006) 65–71 www.elsevier.com/locate/parkreldis
Review
Movement disorders and Creutzfeldt-Jakob disease: A review David Malteˆte a,*, Lucie Guyant-Mare´chal a,b, Bruno Mihout a, Didier Hannequin a,b a
Department of Neurology, Rouen University Hospital, Charles Nicolle, 1 Germont Street 76031 Rouen Cedex, France b INSERM U614, Rouen University Hospital-Charles Nicolle, Rouen-France Received 12 July 2005; received in revised form 28 September 2005; accepted 7 October 2005
Abstract Movement disorders are reported in a significant number of patients within the course of Creutzfeldt-Jakob disease (CJD). Although myoclonus is more frequent, dystonia, choreoathetosis, tremor, hemiballismus, and atypical parkinsonian syndromes have also been reported. In this review, we report the principal movement disorders associated with CJD and evaluate their correlations with neuroradiological and neuropathological findings that could in fact suggest a basal ganglia dysfunction. Further studies are warranted in order to clarify these correlations. q 2005 Elsevier Ltd. All rights reserved. Keywords: Movement disorders; Creutzfeldt-Jacob disease; Basal ganglia
Contents 1. 2.
3.
4.
5.
6.
7. 8. 9.
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Myoclonus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1. Epidemiology of myoclonus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2. Clinical features . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Dystonia . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1. Epidemiology of dystonia . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2. Clinical features . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Choreoathetosis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1. Epidemiology of chorea . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2. Clinical features . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Parkinsonism . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.1. Epidemiology of parkinsonism . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.2. Parkinson disease . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.3. Corticobasal degeneration-like . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.4. Progressive supranuclear palsy-like . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.5. Frontotemporal dementia and parkinsonism . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Tremor . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.1. Epidemiology of tremor . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.2. Clinical features . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Neuroradiological abnormalities . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Pathophysiology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Treatment of movement disorders . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
* Corresponding author. Tel.: C33 2 32 88 87 40; fax: C33 2 32 88 87 41. E-mail address: [email protected] (D. Malteˆte).
1353-8020/$ - see front matter q 2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.parkreldis.2005.10.004
66 66 66 66 66 66 66 67 67 67 67 67 67 67 67 67 68 68 68 68 68 69
D. Malteˆte et al. / Parkinsonism and Related Disorders 12 (2006) 65–71
66
10.
Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 69 Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 69 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 69
1. Introduction Creutzfeldt-Jakob disease (CJD) is a rare neurodegenerative disease that is mainly characterized by rapidly progressive dementia, myoclonus, ataxia and visual disturbances, extrapyramidal and pyramidal involvement, as well as a kinetic mutism [1–3]. Several movement disorders including myoclonus, dystonia, choreoathetosis, tremor, hemiballismus, ‘ill-defined complex’ and atypical parkinsonian syndromes, i.e. corticobasal degeneration (CBD) and supranuclear palsy (PSP), have been described in a significant number of patients with sporadic, familial or new variant of CJD (v-CJD) [4–6]. Basically, the frequency of movement disorders increase with disease duration, but they sometimes occur at an early stage [2], and have been described as initial and/or isolated manifestations of the illness. Classical neuropathological [1,7] and neuroradiological abnormalities [8–10] involve either cortical areas or basal ganglia. In this article, we review the more frequent movement disorders associated with CJD and discuss their correlations with radiological and pathological findings which may suggest a basal ganglia dysfunction.
2. Myoclonus 2.1. Epidemiology of myoclonus Myoclonus is by far the movement disorder most commonly associated with sporadic, familial and new variant CJD [5,7]. Jerks are focal or generalized, have been reported to occur in 82–100% of cases during the course of the disease, and in the majority of advanced forms whatever the genotype [2,4,11]. Myoclonus develops earlier in patients with methionine/methionine (MM) or methionine/valine (MV) at codon 129 of the prion protein gene (PRNP) and with scrapie variant of prion protein PrPSc type 1 [11,12]. Although rare, seizures can also occur even as an early manifestation [13–15]. 2.2. Clinical features Myoclonic jerks are often diffuse, generalized, relatively rhythmic and, associated with periodic sharp-wave EEG activity. They are emphasized by noise and/or sensitive stimuli (startle myoclonus), and can persist during sleep [1,4,16]. They can also be associated with other movement disorders such as, athetoid movements of the fingers [17], alien hand syndrome [18] or dystonic posturing [16]. In these cases, myoclonus jerks are frequently asymmetric,
affecting the distal extremity of upper or lower limb, and can occur early within the course of the disease. Matsunaga et al. described one patient with unusual arrhythmic, actionactivated jerks causing brief postural lapses in the bilateral upper and lower extremities [19]. The electrophysiological study was consistent with a complex negative myoclonus. Seizures are rare in patients with CJD. In major series of definite CJD patients, seizures were reported in 0.4% on clinical presentation and in 8–25% during clinical course [4,11]. They mainly occur at the later stages of the illness and more frequently in the MM1 and MV1 sporadic CJD genotypes [11]. Usually resistant to antiepileptic drugs, they may be generalized or partial [4,20,21]. Epilepsia partialis continua, clinically defined as continuous focal jerking affecting a body part, has also been reported as an initial manifestation in some single sporadic CJD cases [11,13,15].
3. Dystonia 3.1. Epidemiology of dystonia Dystonia, i.e. sustained, inappropriate, twisted posture at rest or during action [22], is listed in the revised diagnostic criteria for possible vCJD (Criteria II D, World Health Organization, 2001) [7,23]. It has also been observed, in many cases of sporadic or familial CJD, as an isolated feature or associated with complex movement disorders. 3.2. Clinical features Dystonia as an early symptom in sporadic or familial CJD is rare, usually unilateral and with distal distribution [12,16,17,24]. Dystonic posture can be focal, affecting the upper limb or the neck [24–27]; segmental as described by Kaneko et al. in a sporadic CJD patient who presented with torsion of the shoulders and the trunk when walking [28]; or hemidystonia as reported in a single case by Maltete et al. [29]. Sethi et al. described a sporadic CJD patient first presenting with a right blepharospasm and left hand dystonic posture. Generalized dystonia has been more commonly reported at the later stage of the disease and is sometimes preceded by focal or hemidystonia that had progressively worsened [25,29]. In the majority of cases, dystonia is associated with other movement disorders such as focal jerk myoclonus restricted to the dystonic limb [24], choreoathetoid movements [16,26,30], postural tremor [24], alien limb [27] or bradykinesia [16].
D. Malteˆte et al. / Parkinsonism and Related Disorders 12 (2006) 65–71
4. Choreoathetosis 4.1. Epidemiology of chorea Choreoathetosis is defined as rapid (chorea) or slow (athetosis) involuntary movements of the fingers or toes which are irregular, non-rhythmic and purposeless [22]. A psychiatric presentation with painful, distal, sensory disturbances, ataxia, and cognitive decline represents the classical characteristic of vCJD [7,23]. Involuntary movements, such as chorea, dystonia or myoclonus, may however occur in non-negligible vCJD cases and are considered as criteria. Although rare, choreoathetosis and ‘other dyskinesias’ have also been reported in sporadic CJD patients [30] occurring more frequently and earlier when associated with the MM1 genotype [11]. 4.2. Clinical features Chorea has been reported as a later stage characteristic in 20 out of 35 definite vCJD [7]. It has often appeared prior to myoclonus, is superimposed with a variety of involuntary movements, such as dystonic postures [30], or athetosis [26], and increased the like hood of vCJD diagnosis. Kaneko et al. reported the case of a 68-year-old man who presented with progressive visual disturbance, gait disorders and athetosis in bilateral fingers associated with shoulder and trunk torsion. CJD diagnosis was suspected due to sub-acute dementia, myoclonus and typical EEG pattern [28]. Recently, two cases of definite vCJD were reported with very early stage generalized and continuous chorea interfering with daily life activities. The movement disorder was the initial and prominent symptom or occurred rapidly after a period of behavioural disturbance [31,32]. 5. Parkinsonism 5.1. Epidemiology of parkinsonism Extrapyramidal syndrome (especially akinetic mutism) is a classical characteristic of the terminal stages of sporadic CJD [11] or vCJD [4,7]. Atypical parkinsonism may however occur as an initial presentation. Gait disorders and rigidity often associated with other signs, i.e. alien limb or supranuclear palsy, could be considered similar to Parkinson-plus syndromes (respectively, corticobasal degeneration and progressive supranuclear palsy). Subacute progression of the symptoms, rapidly combined with cognitive decline and generalized myoclonus, was nevertheless suggestive of CJD.
67
parkinsonism [33]. Neuropathological evaluation revealed features of both sporadic CJD and Parkinson’s disease. 5.3. Corticobasal degeneration-like Alien hand is a rare and striking phenomenon defined as ‘a patient’s failure to recognize the action of one of his hands as his own’ [34]. It is usually accompanied by a combination of involuntary movement disorders (dystonia, myoclonus, choreoathetosis) of the hand and has been well described in CBD. Accuracy of clinical diagnosis of CBD is nevertheless unsatisfactory with a low sensitivity and falsenegative misdiagnoses, particularly with PSP, have been reported [35,36]. In fact, in a series of 17 patients with clinical CBD, only 9 had compatible neuropathological examination whereas 2 had definite CJD [37]. Several authors have provided examples of CJD patients with atypical history of CBD, particularly with sub-acute alien limb and superimposed involuntary movements [17,27,38–40]. MacGowan et al., were the first to report two patients with definite CJD who presented with left alien hand [18]. Both patients complained of focal, stimulus sensitive myoclonus, severe sensory ataxia and proprioceptive dysfunction. Finally, corticobasal degeneration-like syndrome has been described at initial presentation in two different familial CJD [41,42]. 5.4. Progressive supranuclear palsy-like Typical PSP is defined by the association of an a kinetic rigid syndrome with vertical supranuclear ophtalmoplegia, early falls, and levodopa unresponsiveness which progresses slowly with a mean disease duration of approximately 7 years [43]. Rare patients with history of clinically PSP have been finally diagnosed as having definite CJD. Nevertheless, supranuclear gaze palsy may appear as a key characteristic in some familial CJD [44,45]. Kawasaki et al. first reported a definite sporadic CJD case of a 64-year-old man with a 53 months history of progressive dementia and clinical features of progressive supranuclear palsy-like syndrome and dysautonomia [46]. One case reported by Shimamura et al. [47] and two additional cases by Joseph et al. [48] complained of subacute vertical supranuclear opthalmoplegia, unresponsive symmetric parkinsonism (especially axial rigidity) with disease duration between 10 and 29 months. In a series of 35 vCJD, 14 patients presented with upgaze paresis [7]. Clinical a typical CJD with early supranuclear gaze palsy but with no myoclonus or EEG abnormalities have also been described in familial CJD cases caused by 200 Lys mutation of the prion protein gene (PRNP) [45].
5.2. Parkinson disease 5.5. Frontotemporal dementia and parkinsonism Parkinson disease and sporadic CJD has been a fortuitous association reported in a single 64-year-old woman with a previous 4 year history of progressive dementia and
Frontotemporal dementia and parkinsonism linked to chromosome 17 (FTD-17) is an autosomal dominant
68
D. Malteˆte et al. / Parkinsonism and Related Disorders 12 (2006) 65–71
disorder that is mainly characterized by abnormal behaviour and disturbed executive function combined with common parkinsonian characteristics. The symptoms often begins insidiously, typically in the fifth decade, and the duration of the disease varies in a range of 3–30 years. The behavioural disturbances and parkinsonian syndrome, in a familial CJD associated with a PRNP T183A mutation were comparable to FTDP-17 [49]. Nevertheless, the shorter familial CJD duration (mean disease duration: 4 years, ranging from 2 to 9 years) differed from the classical disease progression in FTDP-17 [50].
6. Tremor 6.1. Epidemiology of tremor Tremor is usually described in the early features of sporadic CJD [12]. This should be differentiated from myoclonic jerks or cerebellar dysmetria. 6.2. Clinical features The tremor can be uni-or bilateral, kinetic or postural and involves the upper or lower limbs. When at rest, it is commonly irregular with superimposed dystonic posture or myoclonus [17,24].
7. Neuroradiological abnormalities Neuroradiological abnormalities suggest dysfunction of the basal ganglia in CJD. Hyper-intensities in the posterior (pulvinar) and in the dorsomedial thalamic nuclei, and to a lesser extent in the caudate head, on fluid-attenuatedinversing-recovery (FLAIR) MRI sequences, are striking in vCJD [51]. These so called ‘pulvinar and hockey-stick’ signs have been reported with a sensitivity of 68–90% and specificity of 100% [51,52]. They are listed in the revised diagnostic criteria for possible vCJD (Criteria II D, World Health Organization, 2001) [7,23]. Distribution of the neuropathological lesions in vCJD, i.e. vacuolation, neuronal loss, and astrocytosis involve posterior thalamic nuclei, with a higher degree of astrocytosis in the pulvinar [51]. Conversely, symmetric bilateral, hyper-intense signal changes in the basal ganglia on T2-weighted and proton density-weighted MRIs have been observed in 67–100% of the patients with sporadic CJD [8,10]. These abnormalities more frequently involved the caudate nuclei and putamina and to a lesser extent thalami and pallidi. In a recent retrospective study, Cambier et al. showed that EEG and FLAIR MRI findings were correlated with lateralized or focal neurologic dysfunction in CJD [53]. In eight patients, five presented with asymmetric upper extremity myoclonic posturing and controlateral
radiological abnormalities. The sporadic CJD case with an early left hemidystonia that we previously reported was associated with a controlateral hyperintensity, in putamen and caudate nucleus, on diffusion-weighted MRI [29]. Furthermore, the radiological findings in three patients with atypical history of CBD and left abnormal involuntary movement (alien limb, dystonia, athetosis) involved both right putamen and right caudate nucleus [17,38,40].
8. Pathophysiology Abnormal involuntary movements (i.e. myoclonus, dystonia, tremor and choreathetosis) can be consecutive to lesions of various structures including the striato-pallidal complex, the mesencephalon and the thalamus [54,55]. The thalamus, nucleus caudate and putamen are the most commonly non-cortical area affected by CJD lesions [1]. Some abnormal involuntary movements have been therefore considered to be consecutive to specific basal ganglia dysfunction. Thus, disturbances of inhibitory GABAergic mechanisms have been suggested to explain the typical myoclonus observed in CJD [56,57]. Myoclonus is often related to EEG abnormalities, including slowing of the background rhythms with diffuse or generalized periodic sharp wave complexes [58–60]. The reticular thalamic nucleus, particularly via its inhibitory GABAergic neurones, serves as a pacemaker, generating highly synchronous electric activity. Recently, Tschampa et al. showed that sporadic CJD patients with typical EEG changes and myoclonus, had a predominant loss of inhibitory neurones in the reticular thalamus [61]. This finding appears to be in agreement with the report of focal myoclonus observed after posterior thalamic injury [62]. It has therefore been suggested that thalamic lesions, observed both in sporadic, familial or vCJD could increase the electrical synchronicity responsible for myoclonus genesis. Symptomatic dystonia is more particularly attributed to lesions that affect (i) most frequently the striatopallidal complex, (especially the putamen), and the thalamus; (ii) occasionally the brainstem, the caudate nucleus and the globus pallidus [55,63,64]. The majority of patients who presented with isolated or movement disorders-associated dystonia had typical CJD lesions in basal ganglia [25,30]. Chorea was reported after lesions affecting the caudate nucleus [55], posterior thalamic stroke [65,66] or proprioceptive sensory loss [67]. Thalamic involvement is characterized by the association of chorea with severe sensory deficit and/or painful sensory symptoms and severe ataxia [65]. Similar combined clinical features described in vCJD patients, associated with the frequent neuroradiological basal ganglia abnormalities strongly suggest a shared underlying thalamic dysfunction. Parkinsonism can be caused by bilateral lesions of the basal ganglia affecting the lentiform nucleus, either
D. Malteˆte et al. / Parkinsonism and Related Disorders 12 (2006) 65–71
the globus pallidus or the putamen, or by dopaminergic nigrostriatal pathway deficiency [55]. Neuropathological examination performed in two patients presenting with doparesistant parkinsonism and PSP-like features [48] revealed marked neuronal loss and gliosis with minimal spongiform changes in the substantia nigra suggesting a dopaminergic nigrostriatal pathway dysfunction. The pathogenesis of the alien limb in CJD remains unknown. This phenomenon has been observed after callosal, cortical, and thalamic injuries and may be due to vascular, traumatic or degenerative diseases. Distinct forms of alien limb, especially callosal and frontal forms, are characterized by different types of movement disorders affecting respectively, the non-dominant or dominant hand [68]. All the reported CJD patients were right-handed with a left alien limb and most of them complained of sensitive disorders, gait impairment and focal dystonia and/or myoclonus, thus mimicking numerous symptoms of corticobasal degeneration. A mixed cortical and thalamic dysfunction is therefore likely responsible for this phenomenon. Presence of action or intention tremor due to thalamic injuries has now been recognized [64,65,69]. It is often made by mixed irregular, jerky, postural, kinetic, oscillatory movements of the arm similar to those observed in CJD and is considered to be consecutive to abnormal functioning of the cerebello-thalamic pathways [64].
69
Pentosan polysulfate (PPS) has been shown to prevent the propagation of the abnormal isoform of the prion protein in cell culture model. A 20-year-old man with vCJD was treated with cerebroventricular infusion of PPS that transitory reduced myoclonus [70].
10. Conclusion Approximately 90% of the patients present movement disorders during the course of CJD, especially generalized myoclonus in the advanced stage [2]. Other focal involuntary movements are nevertheless described, although more rarely, whatever the CJD form. In many cases, the clinical presentations resemble neurodegenerative diseases, however, the sub-acute evolution, occurrence of progressive dementia, finally combined with generalized myoclonus suggest a prion disorder. The frequent basal ganglia involvement and its dysfunction appear to be a key factor in the pathogenesis of these involuntary movements. Nevertheless, the lower frequency of movement disorders, except for myoclonus, seems intriguing as regards with the high radiological and neuropathological basal ganglia involvement. Phenotypic heterogeneity could possibly explain the variability of movement disorders and the more recent application of FLAIR and diffusion-weighted MRI sequences could improve the detection of CJD lesions to clarify the correlations between diverse movement disorders and basal ganglia involvement.
9. Treatment of movement disorders Acknowledgements Just as movement disorders accompanying CJD have been rarely specifically studied the effects of treatment remained obscure. Movement disorders usually occur later in the course of the disease, but some patients with early involuntary movements, had received empirical treatment. Thus, one patient was treated by oral prednisone (60 mg/day) with no efficacy on focal dystonia [24] while the parkinsonism of two patients with PSP-like syndrome, did not respond to high doses of levodopa treatment [48]. Choreic and dystonic posture have been transitory diminished by low dose of haloperidol treatment (1.5 mg/day) [15]. Seizures, i.e. epilepsia partialis continua and complex partial status epilepticus, were in most cases resistant to classic antiepileptic drugs [4,14,15,20,21]. Epileptiform discharges were sometimes attenuated or abolished by intravenous diazepam but without clinical improvement [21]. The patient reported by Parry et al. presented with complex partial status epilepticus initially sensitive to an association of phenytoin and clonazepam (4 mg per day) but subsequently resistant to valproic acid and lamotrigine [14]. The involuntary jerking movements presented by the patient described by Lee et al. resisted successive trials of valproate, topiramate, gabapentin, lamotrigine and lorazepam [13].
The authors are grateful to Richard Medeiros, Rouen University Hospital Medical Editor, for his valuable advice in editing the manuscript.
References [1] Masters CL, Richardson EP. Subacute spongiform encephalopathy (Creutzfeldt-Jakob disease). The nature and progression of spongiform change. Brain 1978;101:333–44. [2] Will RG, Matthews WB. A retrospective study of Creutzfeldt-Jakob disease in England and Wales 1970–79. 1. Clinical features. J Neurol Neurosurg Psychiatry 1984;47:134–40. [3] Zerr I, Pocchiari M, Collins S, Brandel JP, de Pedro Cuesta J, Knight RS, Bernheimer H, Cardone F, Delasnerie-Laupretre N, Cuadrado Corrales N, Ladogana A, Bodemer M, Fletcher A, Awan T, Ruiz Bremon A, Budka H, Laplanche JL, Will RG, Poser S. Analysis of EEG and CSF 14-3-3 proteins as aids to the diagnosis of Creutzfeldt-Jakob disease. Neurology 2000;55:811–5. [4] Brown P, Cathala F, Castaigne P, Gadjusek DC. Creutzfeldt-Jakob disease: clinical analysis of consecutive series of 230 neuropathologically verified cases. Ann Neurol 1986;20:597–602. [5] Zeidler M, Stewart GE, Barraclough CR, Bateman DE, Bates D, Colchester AC, Durward W, Flechter NA, Hawkins SA, Mackenzie JM, Will RG. New variant Creutzfeldt-Jakob disease: neurological features and diagnostic tests. Lancet 1997;350:903–7.
70
D. Malteˆte et al. / Parkinsonism and Related Disorders 12 (2006) 65–71
[6] Kovacs GG, Head MW, Bunn T, Laszlo L, Will RG, Ironside JW. Clinicopathological phenotype of codon 129 valine homozygote sporadic Creutzfeldt-Jalob disease. Neuropathol Appl Neurobiol 2000;26:463–72. [7] Will RG, Zeidler M, Stewart GE, Macleod MA, Ironside JW, Cousens SN, Mackenzie J, Estibeiro K, Green AJE, Knight RSG. Diagnosis of new variant Creutzfeldt-Jakob disease. Ann Neurol 2000;47:575–82. [8] Finkenstaedt M, Szudra A, Zerr I, Poser S, Hise JH, Stoebner JM, Weber T. MR imaging of Creutzfeldt-Jakob disease. Radiology 1996; 199:793–8. [9] Bahn M, Parchi P. Abnormal diffusion-weighted magnetic resonance images in Creutzfeldt-Jakob disease. Arch Neurol 1999;56:577–83. [10] Schro¨ter A, Zerr I, Henkel K, Tschampa HJ, Finkenstaedt M, Poser S. Magnetic resonance imaging in the clinical diagnosis of CreutzfeldtJakob disease. Arch Neurol 2000;57:1751–7. [11] Parchi P, Giese A, Capellari S, Brown P, Schulz-Schaeffer W, Windl O, Zerr I, Budka H, Kopp N, Piccardo P, Poser S, Rojiani A, Streichemberger N, Julien J, Vital C, Ghetti B, Gambetti P, Kretzschmar H. Classification of sporadic Creutzfeldt-Jakob disease based on molecular and phenotypic analysis of 300 subjects. Ann Neurol 1999;46:224–33. [12] Marchiori PE, Yasuda N, Azevedo HC, Orfao M, Callegaro D, Yamamoto FI, Scaff M. Creutzfeldt-Jakob disease. A survey of 14 patients. Arq Neuropsiquiatr 1996;54:577–83. [13] Lee K, Haight E, Olejniczak P. Epilespia partialis continua in Creutzfeldt-Jakob disease. Acta Neurol Scand 2000;102:398–402. [14] Parry J, Tuch P, Knezevic W, Fabian V. Creutzfeldt-Jakob syndrome presenting as epilepsia partialis continua. J Clin Neurosci 2001;8: 266–8. [15] Donmez B, Cakmur R, Men S, Oztura I, Kitis A. Coexistence of movement disorders and epilepsia partialis continua as the initial signs in probable Creutzfeldt-Jakob disease. Mov Disord 2005;. doi10. 1002/mds.20502 [published online 13 May 2005]. [16] Sethi KD, Hess DC. Creutzfeldt-Jakob’s disease presenting with ataxia and a movement disorder. Mov Disord 2002;17:1097–8. [17] Anschell DJ, Simon DK, Llinas R, Joseph JT. Spongiform encephalopathy mimicking corticobasal degeneration. Mov Disord 2002;17:606–7. [18] Macgowan DJL, Delantry N, Petito F, Edgar M, Mastrianni J, DeArmond SJ. Isolated myoclonic alien hand as the sole presentation of pathologically established Creutzfeldt-Jakob disease: a report of two patients. J Neurol Neurosurg Psychiatry 1999;63:404–7. [19] Matsunaga K, Uozumi T, Akamatsu N, Nagashio Y, Qingrui L, Hashimoto T, Tsuji S. Negative myoclonus in Creutzfeldt-Jakob disease. Clin Neurophysiol 2000;111:471–6. [20] Burger LJ, Rowan AJ, Goldensohn ES. Creutzfeldt-Jakob disease: an electroencephalographic study. Arch Neurol 1972;26:428–33. [21] Rees JH, Smith SJ, Kullman DM, Hirsch NP, Howard RS. Creutzfeldt-Jakob disease presenting as complex partial status epilepticus: a report of two cases. J Neurol Neurosurg Psychiatry 1999;66:406–13. [22] Fahn S. Phenomenology of movement disorders. In: Fahn S, Marsden CD, Jankovic J, editors. Seventh annual course: a comprehensive review of movement disorders for the clinical practitioner. New York: Columbia University; 1997. p. 3–61. [23] The revision of the surveillance case definition for variant CreutzfeldtJakob disease (vCJD). [WHO/CDS/CSR/EPH/2001.5]. Geneva, Switzerland: World Health Organization; 2001. [24] Hellmann MA, Melamed E. Focal dystonia as the presenting sign in Creutzfeldt-Jakob disease. Mov Disord 2002;17:1097–8. [25] Roos R, Gajdusek DC, Gibbs CJ. The clinical characteristics of transmissible Creutzfeldt-Jakob disease. Brain 1974;96:1–20. [26] Scully RE, Mauk E, McNeely BV. Case records of the Massachusetts General Hospital. N Engl J Med 1983;309:1440–9.
[27] Inzelberg R, Nisipeanu P, Blumen SC, Carasso RL. Alien hand sign in Creutzfeldt-Jakob disease. J Neurol Neurosurg Psychiatry 2000;68: 103–4. [28] Kaneko A, Takei K, Enomoto K, Mitsui T, Nomura K, Iwasaki S, Maruki T, Shimazu K. A case of Creutzfeldt-Jakob disease exhibiting athetosis in the early stage. No To Shinkei 1999;51:887–90. [29] Malteˆte D, Guyant-Mare´chal L, Ge´rardin E, Laquerrie`re A, Martinaud O, Mihout B, Hannequin D. Hemidystonia as initial manifestation of sporadic Creutzfeldt-Jakob disease. Eur J Neurol; in press. [30] Zochodne DW, Young GB, McLachlan RS, Gilbert JJ, Vinters HV, Kaufmann JCE. Creutzfeldt-Jakob disease without periodic sharp wave complexes. Neurology 1988;38:1056–60. [31] Bowen J, Mitchell T, Pearce R, Quinn N. Chorea in new variant Creutzfeldt-Jakob disease. Mov Disord 2000;15:1284–5. [32] McKee D, Talbot P. Chorea as a presenting feature of variant Creutzfeldt-Jakob disease. Mov Disord 2003;18:837–8. [33] Iida T, Doh-Ura K, Kawashima T, Abe H, Iwaki T. An atypical case of sporadic Creutzfeldt-Jakob disease with Parkinson’s disease. Neuropathology 2001;21:294–7. [34] Levine DN. The alien hand. In: Joseph AB, Young RR, editors. Movement disorder in neurology and neuropsychiatry. Oxford: Blackwell; 1999. p. 645–9. [35] Litvan I, Agid Y, Calne D, Goetz C, Jankovic J, Wenning GK, Lai EC, Verny M, Ray-Chaudhuri K, McKee A, Jellinger K, Pearce RK, Bartko JJ. Accuracy of the clinical diagnosis of corticobasal degeneration: a clinicopathologic study. Neurology 1997;48:119–25. [36] Mahapatra RK, Edwards MJ, Schott JM, Bhatia KP. Corticobasal degeneration. Lancet Neurol 2004;3:736–43. [37] Josephs KA, Tang-Wai DF, Edland SD, Knopman DS, Dickson DW, Parisi JE, Petersen RC, Jack CR, Boeve BF. Correlation between antemortem magnetic resonance imaging findings and pathologically confirmed corticobasal degeneration. Arch Neurol 2004;61:1881–4. [38] Cannard KR, Galves-Jimenez N, Watts RL. Creutzfeldt-Jakob disease presenting and evolving as rapidly progressive corticobasal degeneration. Neurology 1998;50:A95–6. [39] Deramecourt V, Girard-Buttaz I, Verier A. A case of spongiform encephalopathy mimicking cortico-basal degeneration. Rev Neurol 2004;160:592–4. [40] Kleiner-Fisman G, Bergeron C, Lang AE. Presentation of CreutzfeldtJakob disease as acute coticobasal degeneration syndrome. Mov Disord 2004;19:948–9. [41] Kovacs GG, Trabattoni G, Hainfellner JA, Ironside JW, Knight RS, Budka H. Mutations of the prion protein gene phenotypic spectrum. J Neurol 2002;249:1567–82. [42] Oberndorfer S, Urbanits S, Lahrmann H, Jarius C, Albrecht G, Grisold W. Familial Creutzfeldt-Jakob disease initially presenting with alien hand syndrome. J Neurol 2002;249:631–2. [43] Litvan I, Agid Y, Calne D, Campbell G, Dubois B, Duvoisin RC, Goetz CG, Golbe LI, Grafman J, Growdon JH, Hallett M, Jankovic J, Quinn NP, Tolosa E, Zee DS. 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. [44] Bertoni JM, Label LS, Sackelleres JC, Hicks SP. Supranuclear gaze palsy in familial Creutzfeldt-Jakob disease. Arch Neurol 1983;40: 618–22. [45] Bertoni JM, Brown P, Goldfarb LG, Rubenstein R, Gajdusek DC. Familial Creutzfeldt-Jakob disease (codon 200 mutation) with supranuclear palsy. JAMA 1992;268:2413–5. [46] Kawasaki K, Wakabayashi K, Kawakami A, Higuchi M, Kitamoto T, Tsuji S, Takabashi H. Thalamic form of Creutzfeldt-Jakob disease or fatal insomnia? Report of sporadic case with normal prion protein genotype Acta Neuropathol 1997;93:317–22. [47] Shimamura M, Uyama E, Hirano T, Murakami T, Mita S, Kitamoto T, Uchino M. A unique case of sporadic Creutzfeldt-Jakob disease presenting as progressive supranuclear palsy. Intern Med 2003;42: 195–8.
D. Malteˆte et al. / Parkinsonism and Related Disorders 12 (2006) 65–71 [48] Josephs KA, Tsuboi Y, Dickson DW. Creutzfeldt-Jakob disease presenting as progressive supranuclear palsy. Eur J Neurol 2004;11: 343–6. [49] Nitrini R, Teixeira da Silva LS, Rosemberg S, Caramelli P, Mestrinelli Carrilho PE, Lughetti P, Passos-Bueno MR, Zatz M, Albrecht S, LeBlanc A. Prion disease resembling frontotemporal dementia and parkinsonism linked to chromosome 17. Arq Neuropsiquiatr 2001;59:161–4. [50] Foster NL, Wilhelmsen K, Sima AA, Jones MZ, D’Amato CJ, Gilman S. Frontotemporal dementia and parkinsonism linked to chromosome 17: a consensus conference. Ann Neurol 1997;41: 706–15. [51] Collie DA, Summers DM, Sellar RJ, Ironside JW, Cooper S, Zeidler M, Knight R, Will RG. Diagnosing variant CreutzfeldtJakob disease with the pulvinar sign: MR imaging findings in 86 neuropathologically confirmed cases. Am J Neuroradiol 2003;24: 1560–9. [52] Zeidler M, Sellar RJ, Collie DA, Knight R, Stewart G, Macleod MA, Ironside JW, Cousens S, Colchester AC, Hadley DM, Will RG. The pulvinar sign on magnetic resonance imaging in variant creutzfeldtJakob disease. Lancet 2000;355:1412–8. [53] Cambier DM, Kantarci K, Worrell GA, Westmoreland BF, Aksamit AJ. Lateralized and focal clinical, EEG, and FLAIR MRI abnormalities in Creutzfeldt-Jakob disease. Clin Neurophysiol 2003; 114:1724–8. [54] Lee MS, Marsden CD. Movement disorders following lesions of the thalamus or subthalamic region. Mov Disord 1994;9:493–507. [55] Bhatia KP, Marsden CD. Behavioral and motor consequences of focal lesions of the basal ganglia in man. Brain 1994;117:859–79. [56] Guentchev M, Groschup MH, Kordek R, Liberski PP, Budka H. Severe, early and selective loss if subpopulation of GABAergic inhibitory neurons in experimental transmissible spongiform encephalopathies. Brain Pathol 1998;8:615–23. [57] Belichenko PV, Miklossy J, Belser B, Budka H, Celio MR. Early destruction of the extracellular matrix around parvalbumin-immunoreactive interneurons in Creutzfeldt-Jakob disease. Neurobiol Dis 1999;6:269–79.
71
[58] Au WJ, Gabor AJ, Vijayan N, Markand ON. Periodic lateralized epileptiform complexes in Creutzfeldt-Jakob disease. Neurology 1980;30:611–7. [59] Shibasaki H, Motomura S, Yamashita Y, Shii H, Kuroiwa Y. Periodic synchronous discharge and myoclonus in Creutzfeldt-Jakob disease: diagnostic application of jerk-locked averaging method. Ann Neurol 1981;9:150–6. [60] Steinhoff BJ, Zerr I, Glatting M, Schulz-Schaeffer W, Poser S. Diagnostic value of periodic complexes in Creutzfeldt-Jakob disease. Ann Neurol 2004;56:702–8. [61] Tschampa HJ, Herms JW, Schulz-Schaeffer WJ, Maruschak B, Windl O, Jastrow U, Zerr I, Steinhoff BJ, Poser S, Kretschmar HA. Clinical findings in sporadic Creutzfeldt-Jakob disease correlate with thalamic pathology. Brain 2002;125:2558–66. [62] Gatto EM, Zurru MC, Rugilo C, Mitre S, Pardal AM, Martinez M, Pardal MM. Focal myoclonus associated with posterior thalamic hematoma. Mov Disord 1998;13:182–4. [63] Marsden CD, Obeso JA, Zarrang JJ, Lang AE. The anatomical basis of symptomatic hemidystonia. Brain 1985;108:463–83. [64] Lehe´ricy S, Vidailhet M, Dormont D, Piero L, Chiras J, Mazetti P, Marsault C, Agid Y. Sriatopallidal and thalamic dystonia: an MR anatomoclinical study. Arch Neurol 1996;53:241–50. [65] Kim JS. Delayed onset mixed involuntary movements after thalamic stroke. Clinical, radiological and pathophysiological findings. Brain 2001;124:299–309. [66] Dietl T, Auer DP, Modell S, Lechner C, Trenkwalder C. Involuntary vocalisations and complex hyperkinetic movement disorder following left side thalamic haemorrhage. Behav Neurol 2003;14:99–102. [67] Sharp FR, Rando TA, Greenberg SA, Brown L, Sagar SM. Pseudochoreoathetosis. Movements associated with loss of proprioception. Arch Neurol 1994;51:1103–9. [68] Feinberg TE, Schindler RJ, Flanagan NG, Haber LD. Two alien hand syndromes. Neurology 1992;42:19–24. [69] Soler R, Vivancos F, Munoz-Torrero JJ, Arpa J, Barreiro P. Postural tremor after thalamic infarction. Eur Neurol 1999;42:180–1. [70] Todd NV, Morrow J, Doh-ura K, Dealler S, O’Hare S, Farling P, Duddy M, Rainov NG. Cerebroventricular infusion of pentosan polysulfate in human variant Creutzfeldt-Jakob disease. J Infect 2005; 50:394–6.
Review
Movement disorders and Creutzfeldt-Jakob disease: A review David Malteˆte a,*, Lucie Guyant-Mare´chal a,b, Bruno Mihout a, Didier Hannequin a,b a
Department of Neurology, Rouen University Hospital, Charles Nicolle, 1 Germont Street 76031 Rouen Cedex, France b INSERM U614, Rouen University Hospital-Charles Nicolle, Rouen-France Received 12 July 2005; received in revised form 28 September 2005; accepted 7 October 2005
Abstract Movement disorders are reported in a significant number of patients within the course of Creutzfeldt-Jakob disease (CJD). Although myoclonus is more frequent, dystonia, choreoathetosis, tremor, hemiballismus, and atypical parkinsonian syndromes have also been reported. In this review, we report the principal movement disorders associated with CJD and evaluate their correlations with neuroradiological and neuropathological findings that could in fact suggest a basal ganglia dysfunction. Further studies are warranted in order to clarify these correlations. q 2005 Elsevier Ltd. All rights reserved. Keywords: Movement disorders; Creutzfeldt-Jacob disease; Basal ganglia
Contents 1. 2.
3.
4.
5.
6.
7. 8. 9.
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Myoclonus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1. Epidemiology of myoclonus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2. Clinical features . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Dystonia . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1. Epidemiology of dystonia . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2. Clinical features . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Choreoathetosis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1. Epidemiology of chorea . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2. Clinical features . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Parkinsonism . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.1. Epidemiology of parkinsonism . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.2. Parkinson disease . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.3. Corticobasal degeneration-like . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.4. Progressive supranuclear palsy-like . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.5. Frontotemporal dementia and parkinsonism . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Tremor . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.1. Epidemiology of tremor . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.2. Clinical features . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Neuroradiological abnormalities . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Pathophysiology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Treatment of movement disorders . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
* Corresponding author. Tel.: C33 2 32 88 87 40; fax: C33 2 32 88 87 41. E-mail address: [email protected] (D. Malteˆte).
1353-8020/$ - see front matter q 2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.parkreldis.2005.10.004
66 66 66 66 66 66 66 67 67 67 67 67 67 67 67 67 68 68 68 68 68 69
D. Malteˆte et al. / Parkinsonism and Related Disorders 12 (2006) 65–71
66
10.
Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 69 Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 69 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 69
1. Introduction Creutzfeldt-Jakob disease (CJD) is a rare neurodegenerative disease that is mainly characterized by rapidly progressive dementia, myoclonus, ataxia and visual disturbances, extrapyramidal and pyramidal involvement, as well as a kinetic mutism [1–3]. Several movement disorders including myoclonus, dystonia, choreoathetosis, tremor, hemiballismus, ‘ill-defined complex’ and atypical parkinsonian syndromes, i.e. corticobasal degeneration (CBD) and supranuclear palsy (PSP), have been described in a significant number of patients with sporadic, familial or new variant of CJD (v-CJD) [4–6]. Basically, the frequency of movement disorders increase with disease duration, but they sometimes occur at an early stage [2], and have been described as initial and/or isolated manifestations of the illness. Classical neuropathological [1,7] and neuroradiological abnormalities [8–10] involve either cortical areas or basal ganglia. In this article, we review the more frequent movement disorders associated with CJD and discuss their correlations with radiological and pathological findings which may suggest a basal ganglia dysfunction.
2. Myoclonus 2.1. Epidemiology of myoclonus Myoclonus is by far the movement disorder most commonly associated with sporadic, familial and new variant CJD [5,7]. Jerks are focal or generalized, have been reported to occur in 82–100% of cases during the course of the disease, and in the majority of advanced forms whatever the genotype [2,4,11]. Myoclonus develops earlier in patients with methionine/methionine (MM) or methionine/valine (MV) at codon 129 of the prion protein gene (PRNP) and with scrapie variant of prion protein PrPSc type 1 [11,12]. Although rare, seizures can also occur even as an early manifestation [13–15]. 2.2. Clinical features Myoclonic jerks are often diffuse, generalized, relatively rhythmic and, associated with periodic sharp-wave EEG activity. They are emphasized by noise and/or sensitive stimuli (startle myoclonus), and can persist during sleep [1,4,16]. They can also be associated with other movement disorders such as, athetoid movements of the fingers [17], alien hand syndrome [18] or dystonic posturing [16]. In these cases, myoclonus jerks are frequently asymmetric,
affecting the distal extremity of upper or lower limb, and can occur early within the course of the disease. Matsunaga et al. described one patient with unusual arrhythmic, actionactivated jerks causing brief postural lapses in the bilateral upper and lower extremities [19]. The electrophysiological study was consistent with a complex negative myoclonus. Seizures are rare in patients with CJD. In major series of definite CJD patients, seizures were reported in 0.4% on clinical presentation and in 8–25% during clinical course [4,11]. They mainly occur at the later stages of the illness and more frequently in the MM1 and MV1 sporadic CJD genotypes [11]. Usually resistant to antiepileptic drugs, they may be generalized or partial [4,20,21]. Epilepsia partialis continua, clinically defined as continuous focal jerking affecting a body part, has also been reported as an initial manifestation in some single sporadic CJD cases [11,13,15].
3. Dystonia 3.1. Epidemiology of dystonia Dystonia, i.e. sustained, inappropriate, twisted posture at rest or during action [22], is listed in the revised diagnostic criteria for possible vCJD (Criteria II D, World Health Organization, 2001) [7,23]. It has also been observed, in many cases of sporadic or familial CJD, as an isolated feature or associated with complex movement disorders. 3.2. Clinical features Dystonia as an early symptom in sporadic or familial CJD is rare, usually unilateral and with distal distribution [12,16,17,24]. Dystonic posture can be focal, affecting the upper limb or the neck [24–27]; segmental as described by Kaneko et al. in a sporadic CJD patient who presented with torsion of the shoulders and the trunk when walking [28]; or hemidystonia as reported in a single case by Maltete et al. [29]. Sethi et al. described a sporadic CJD patient first presenting with a right blepharospasm and left hand dystonic posture. Generalized dystonia has been more commonly reported at the later stage of the disease and is sometimes preceded by focal or hemidystonia that had progressively worsened [25,29]. In the majority of cases, dystonia is associated with other movement disorders such as focal jerk myoclonus restricted to the dystonic limb [24], choreoathetoid movements [16,26,30], postural tremor [24], alien limb [27] or bradykinesia [16].
D. Malteˆte et al. / Parkinsonism and Related Disorders 12 (2006) 65–71
4. Choreoathetosis 4.1. Epidemiology of chorea Choreoathetosis is defined as rapid (chorea) or slow (athetosis) involuntary movements of the fingers or toes which are irregular, non-rhythmic and purposeless [22]. A psychiatric presentation with painful, distal, sensory disturbances, ataxia, and cognitive decline represents the classical characteristic of vCJD [7,23]. Involuntary movements, such as chorea, dystonia or myoclonus, may however occur in non-negligible vCJD cases and are considered as criteria. Although rare, choreoathetosis and ‘other dyskinesias’ have also been reported in sporadic CJD patients [30] occurring more frequently and earlier when associated with the MM1 genotype [11]. 4.2. Clinical features Chorea has been reported as a later stage characteristic in 20 out of 35 definite vCJD [7]. It has often appeared prior to myoclonus, is superimposed with a variety of involuntary movements, such as dystonic postures [30], or athetosis [26], and increased the like hood of vCJD diagnosis. Kaneko et al. reported the case of a 68-year-old man who presented with progressive visual disturbance, gait disorders and athetosis in bilateral fingers associated with shoulder and trunk torsion. CJD diagnosis was suspected due to sub-acute dementia, myoclonus and typical EEG pattern [28]. Recently, two cases of definite vCJD were reported with very early stage generalized and continuous chorea interfering with daily life activities. The movement disorder was the initial and prominent symptom or occurred rapidly after a period of behavioural disturbance [31,32]. 5. Parkinsonism 5.1. Epidemiology of parkinsonism Extrapyramidal syndrome (especially akinetic mutism) is a classical characteristic of the terminal stages of sporadic CJD [11] or vCJD [4,7]. Atypical parkinsonism may however occur as an initial presentation. Gait disorders and rigidity often associated with other signs, i.e. alien limb or supranuclear palsy, could be considered similar to Parkinson-plus syndromes (respectively, corticobasal degeneration and progressive supranuclear palsy). Subacute progression of the symptoms, rapidly combined with cognitive decline and generalized myoclonus, was nevertheless suggestive of CJD.
67
parkinsonism [33]. Neuropathological evaluation revealed features of both sporadic CJD and Parkinson’s disease. 5.3. Corticobasal degeneration-like Alien hand is a rare and striking phenomenon defined as ‘a patient’s failure to recognize the action of one of his hands as his own’ [34]. It is usually accompanied by a combination of involuntary movement disorders (dystonia, myoclonus, choreoathetosis) of the hand and has been well described in CBD. Accuracy of clinical diagnosis of CBD is nevertheless unsatisfactory with a low sensitivity and falsenegative misdiagnoses, particularly with PSP, have been reported [35,36]. In fact, in a series of 17 patients with clinical CBD, only 9 had compatible neuropathological examination whereas 2 had definite CJD [37]. Several authors have provided examples of CJD patients with atypical history of CBD, particularly with sub-acute alien limb and superimposed involuntary movements [17,27,38–40]. MacGowan et al., were the first to report two patients with definite CJD who presented with left alien hand [18]. Both patients complained of focal, stimulus sensitive myoclonus, severe sensory ataxia and proprioceptive dysfunction. Finally, corticobasal degeneration-like syndrome has been described at initial presentation in two different familial CJD [41,42]. 5.4. Progressive supranuclear palsy-like Typical PSP is defined by the association of an a kinetic rigid syndrome with vertical supranuclear ophtalmoplegia, early falls, and levodopa unresponsiveness which progresses slowly with a mean disease duration of approximately 7 years [43]. Rare patients with history of clinically PSP have been finally diagnosed as having definite CJD. Nevertheless, supranuclear gaze palsy may appear as a key characteristic in some familial CJD [44,45]. Kawasaki et al. first reported a definite sporadic CJD case of a 64-year-old man with a 53 months history of progressive dementia and clinical features of progressive supranuclear palsy-like syndrome and dysautonomia [46]. One case reported by Shimamura et al. [47] and two additional cases by Joseph et al. [48] complained of subacute vertical supranuclear opthalmoplegia, unresponsive symmetric parkinsonism (especially axial rigidity) with disease duration between 10 and 29 months. In a series of 35 vCJD, 14 patients presented with upgaze paresis [7]. Clinical a typical CJD with early supranuclear gaze palsy but with no myoclonus or EEG abnormalities have also been described in familial CJD cases caused by 200 Lys mutation of the prion protein gene (PRNP) [45].
5.2. Parkinson disease 5.5. Frontotemporal dementia and parkinsonism Parkinson disease and sporadic CJD has been a fortuitous association reported in a single 64-year-old woman with a previous 4 year history of progressive dementia and
Frontotemporal dementia and parkinsonism linked to chromosome 17 (FTD-17) is an autosomal dominant
68
D. Malteˆte et al. / Parkinsonism and Related Disorders 12 (2006) 65–71
disorder that is mainly characterized by abnormal behaviour and disturbed executive function combined with common parkinsonian characteristics. The symptoms often begins insidiously, typically in the fifth decade, and the duration of the disease varies in a range of 3–30 years. The behavioural disturbances and parkinsonian syndrome, in a familial CJD associated with a PRNP T183A mutation were comparable to FTDP-17 [49]. Nevertheless, the shorter familial CJD duration (mean disease duration: 4 years, ranging from 2 to 9 years) differed from the classical disease progression in FTDP-17 [50].
6. Tremor 6.1. Epidemiology of tremor Tremor is usually described in the early features of sporadic CJD [12]. This should be differentiated from myoclonic jerks or cerebellar dysmetria. 6.2. Clinical features The tremor can be uni-or bilateral, kinetic or postural and involves the upper or lower limbs. When at rest, it is commonly irregular with superimposed dystonic posture or myoclonus [17,24].
7. Neuroradiological abnormalities Neuroradiological abnormalities suggest dysfunction of the basal ganglia in CJD. Hyper-intensities in the posterior (pulvinar) and in the dorsomedial thalamic nuclei, and to a lesser extent in the caudate head, on fluid-attenuatedinversing-recovery (FLAIR) MRI sequences, are striking in vCJD [51]. These so called ‘pulvinar and hockey-stick’ signs have been reported with a sensitivity of 68–90% and specificity of 100% [51,52]. They are listed in the revised diagnostic criteria for possible vCJD (Criteria II D, World Health Organization, 2001) [7,23]. Distribution of the neuropathological lesions in vCJD, i.e. vacuolation, neuronal loss, and astrocytosis involve posterior thalamic nuclei, with a higher degree of astrocytosis in the pulvinar [51]. Conversely, symmetric bilateral, hyper-intense signal changes in the basal ganglia on T2-weighted and proton density-weighted MRIs have been observed in 67–100% of the patients with sporadic CJD [8,10]. These abnormalities more frequently involved the caudate nuclei and putamina and to a lesser extent thalami and pallidi. In a recent retrospective study, Cambier et al. showed that EEG and FLAIR MRI findings were correlated with lateralized or focal neurologic dysfunction in CJD [53]. In eight patients, five presented with asymmetric upper extremity myoclonic posturing and controlateral
radiological abnormalities. The sporadic CJD case with an early left hemidystonia that we previously reported was associated with a controlateral hyperintensity, in putamen and caudate nucleus, on diffusion-weighted MRI [29]. Furthermore, the radiological findings in three patients with atypical history of CBD and left abnormal involuntary movement (alien limb, dystonia, athetosis) involved both right putamen and right caudate nucleus [17,38,40].
8. Pathophysiology Abnormal involuntary movements (i.e. myoclonus, dystonia, tremor and choreathetosis) can be consecutive to lesions of various structures including the striato-pallidal complex, the mesencephalon and the thalamus [54,55]. The thalamus, nucleus caudate and putamen are the most commonly non-cortical area affected by CJD lesions [1]. Some abnormal involuntary movements have been therefore considered to be consecutive to specific basal ganglia dysfunction. Thus, disturbances of inhibitory GABAergic mechanisms have been suggested to explain the typical myoclonus observed in CJD [56,57]. Myoclonus is often related to EEG abnormalities, including slowing of the background rhythms with diffuse or generalized periodic sharp wave complexes [58–60]. The reticular thalamic nucleus, particularly via its inhibitory GABAergic neurones, serves as a pacemaker, generating highly synchronous electric activity. Recently, Tschampa et al. showed that sporadic CJD patients with typical EEG changes and myoclonus, had a predominant loss of inhibitory neurones in the reticular thalamus [61]. This finding appears to be in agreement with the report of focal myoclonus observed after posterior thalamic injury [62]. It has therefore been suggested that thalamic lesions, observed both in sporadic, familial or vCJD could increase the electrical synchronicity responsible for myoclonus genesis. Symptomatic dystonia is more particularly attributed to lesions that affect (i) most frequently the striatopallidal complex, (especially the putamen), and the thalamus; (ii) occasionally the brainstem, the caudate nucleus and the globus pallidus [55,63,64]. The majority of patients who presented with isolated or movement disorders-associated dystonia had typical CJD lesions in basal ganglia [25,30]. Chorea was reported after lesions affecting the caudate nucleus [55], posterior thalamic stroke [65,66] or proprioceptive sensory loss [67]. Thalamic involvement is characterized by the association of chorea with severe sensory deficit and/or painful sensory symptoms and severe ataxia [65]. Similar combined clinical features described in vCJD patients, associated with the frequent neuroradiological basal ganglia abnormalities strongly suggest a shared underlying thalamic dysfunction. Parkinsonism can be caused by bilateral lesions of the basal ganglia affecting the lentiform nucleus, either
D. Malteˆte et al. / Parkinsonism and Related Disorders 12 (2006) 65–71
the globus pallidus or the putamen, or by dopaminergic nigrostriatal pathway deficiency [55]. Neuropathological examination performed in two patients presenting with doparesistant parkinsonism and PSP-like features [48] revealed marked neuronal loss and gliosis with minimal spongiform changes in the substantia nigra suggesting a dopaminergic nigrostriatal pathway dysfunction. The pathogenesis of the alien limb in CJD remains unknown. This phenomenon has been observed after callosal, cortical, and thalamic injuries and may be due to vascular, traumatic or degenerative diseases. Distinct forms of alien limb, especially callosal and frontal forms, are characterized by different types of movement disorders affecting respectively, the non-dominant or dominant hand [68]. All the reported CJD patients were right-handed with a left alien limb and most of them complained of sensitive disorders, gait impairment and focal dystonia and/or myoclonus, thus mimicking numerous symptoms of corticobasal degeneration. A mixed cortical and thalamic dysfunction is therefore likely responsible for this phenomenon. Presence of action or intention tremor due to thalamic injuries has now been recognized [64,65,69]. It is often made by mixed irregular, jerky, postural, kinetic, oscillatory movements of the arm similar to those observed in CJD and is considered to be consecutive to abnormal functioning of the cerebello-thalamic pathways [64].
69
Pentosan polysulfate (PPS) has been shown to prevent the propagation of the abnormal isoform of the prion protein in cell culture model. A 20-year-old man with vCJD was treated with cerebroventricular infusion of PPS that transitory reduced myoclonus [70].
10. Conclusion Approximately 90% of the patients present movement disorders during the course of CJD, especially generalized myoclonus in the advanced stage [2]. Other focal involuntary movements are nevertheless described, although more rarely, whatever the CJD form. In many cases, the clinical presentations resemble neurodegenerative diseases, however, the sub-acute evolution, occurrence of progressive dementia, finally combined with generalized myoclonus suggest a prion disorder. The frequent basal ganglia involvement and its dysfunction appear to be a key factor in the pathogenesis of these involuntary movements. Nevertheless, the lower frequency of movement disorders, except for myoclonus, seems intriguing as regards with the high radiological and neuropathological basal ganglia involvement. Phenotypic heterogeneity could possibly explain the variability of movement disorders and the more recent application of FLAIR and diffusion-weighted MRI sequences could improve the detection of CJD lesions to clarify the correlations between diverse movement disorders and basal ganglia involvement.
9. Treatment of movement disorders Acknowledgements Just as movement disorders accompanying CJD have been rarely specifically studied the effects of treatment remained obscure. Movement disorders usually occur later in the course of the disease, but some patients with early involuntary movements, had received empirical treatment. Thus, one patient was treated by oral prednisone (60 mg/day) with no efficacy on focal dystonia [24] while the parkinsonism of two patients with PSP-like syndrome, did not respond to high doses of levodopa treatment [48]. Choreic and dystonic posture have been transitory diminished by low dose of haloperidol treatment (1.5 mg/day) [15]. Seizures, i.e. epilepsia partialis continua and complex partial status epilepticus, were in most cases resistant to classic antiepileptic drugs [4,14,15,20,21]. Epileptiform discharges were sometimes attenuated or abolished by intravenous diazepam but without clinical improvement [21]. The patient reported by Parry et al. presented with complex partial status epilepticus initially sensitive to an association of phenytoin and clonazepam (4 mg per day) but subsequently resistant to valproic acid and lamotrigine [14]. The involuntary jerking movements presented by the patient described by Lee et al. resisted successive trials of valproate, topiramate, gabapentin, lamotrigine and lorazepam [13].
The authors are grateful to Richard Medeiros, Rouen University Hospital Medical Editor, for his valuable advice in editing the manuscript.
References [1] Masters CL, Richardson EP. Subacute spongiform encephalopathy (Creutzfeldt-Jakob disease). The nature and progression of spongiform change. Brain 1978;101:333–44. [2] Will RG, Matthews WB. A retrospective study of Creutzfeldt-Jakob disease in England and Wales 1970–79. 1. Clinical features. J Neurol Neurosurg Psychiatry 1984;47:134–40. [3] Zerr I, Pocchiari M, Collins S, Brandel JP, de Pedro Cuesta J, Knight RS, Bernheimer H, Cardone F, Delasnerie-Laupretre N, Cuadrado Corrales N, Ladogana A, Bodemer M, Fletcher A, Awan T, Ruiz Bremon A, Budka H, Laplanche JL, Will RG, Poser S. Analysis of EEG and CSF 14-3-3 proteins as aids to the diagnosis of Creutzfeldt-Jakob disease. Neurology 2000;55:811–5. [4] Brown P, Cathala F, Castaigne P, Gadjusek DC. Creutzfeldt-Jakob disease: clinical analysis of consecutive series of 230 neuropathologically verified cases. Ann Neurol 1986;20:597–602. [5] Zeidler M, Stewart GE, Barraclough CR, Bateman DE, Bates D, Colchester AC, Durward W, Flechter NA, Hawkins SA, Mackenzie JM, Will RG. New variant Creutzfeldt-Jakob disease: neurological features and diagnostic tests. Lancet 1997;350:903–7.
70
D. Malteˆte et al. / Parkinsonism and Related Disorders 12 (2006) 65–71
[6] Kovacs GG, Head MW, Bunn T, Laszlo L, Will RG, Ironside JW. Clinicopathological phenotype of codon 129 valine homozygote sporadic Creutzfeldt-Jalob disease. Neuropathol Appl Neurobiol 2000;26:463–72. [7] Will RG, Zeidler M, Stewart GE, Macleod MA, Ironside JW, Cousens SN, Mackenzie J, Estibeiro K, Green AJE, Knight RSG. Diagnosis of new variant Creutzfeldt-Jakob disease. Ann Neurol 2000;47:575–82. [8] Finkenstaedt M, Szudra A, Zerr I, Poser S, Hise JH, Stoebner JM, Weber T. MR imaging of Creutzfeldt-Jakob disease. Radiology 1996; 199:793–8. [9] Bahn M, Parchi P. Abnormal diffusion-weighted magnetic resonance images in Creutzfeldt-Jakob disease. Arch Neurol 1999;56:577–83. [10] Schro¨ter A, Zerr I, Henkel K, Tschampa HJ, Finkenstaedt M, Poser S. Magnetic resonance imaging in the clinical diagnosis of CreutzfeldtJakob disease. Arch Neurol 2000;57:1751–7. [11] Parchi P, Giese A, Capellari S, Brown P, Schulz-Schaeffer W, Windl O, Zerr I, Budka H, Kopp N, Piccardo P, Poser S, Rojiani A, Streichemberger N, Julien J, Vital C, Ghetti B, Gambetti P, Kretzschmar H. Classification of sporadic Creutzfeldt-Jakob disease based on molecular and phenotypic analysis of 300 subjects. Ann Neurol 1999;46:224–33. [12] Marchiori PE, Yasuda N, Azevedo HC, Orfao M, Callegaro D, Yamamoto FI, Scaff M. Creutzfeldt-Jakob disease. A survey of 14 patients. Arq Neuropsiquiatr 1996;54:577–83. [13] Lee K, Haight E, Olejniczak P. Epilespia partialis continua in Creutzfeldt-Jakob disease. Acta Neurol Scand 2000;102:398–402. [14] Parry J, Tuch P, Knezevic W, Fabian V. Creutzfeldt-Jakob syndrome presenting as epilepsia partialis continua. J Clin Neurosci 2001;8: 266–8. [15] Donmez B, Cakmur R, Men S, Oztura I, Kitis A. Coexistence of movement disorders and epilepsia partialis continua as the initial signs in probable Creutzfeldt-Jakob disease. Mov Disord 2005;. doi10. 1002/mds.20502 [published online 13 May 2005]. [16] Sethi KD, Hess DC. Creutzfeldt-Jakob’s disease presenting with ataxia and a movement disorder. Mov Disord 2002;17:1097–8. [17] Anschell DJ, Simon DK, Llinas R, Joseph JT. Spongiform encephalopathy mimicking corticobasal degeneration. Mov Disord 2002;17:606–7. [18] Macgowan DJL, Delantry N, Petito F, Edgar M, Mastrianni J, DeArmond SJ. Isolated myoclonic alien hand as the sole presentation of pathologically established Creutzfeldt-Jakob disease: a report of two patients. J Neurol Neurosurg Psychiatry 1999;63:404–7. [19] Matsunaga K, Uozumi T, Akamatsu N, Nagashio Y, Qingrui L, Hashimoto T, Tsuji S. Negative myoclonus in Creutzfeldt-Jakob disease. Clin Neurophysiol 2000;111:471–6. [20] Burger LJ, Rowan AJ, Goldensohn ES. Creutzfeldt-Jakob disease: an electroencephalographic study. Arch Neurol 1972;26:428–33. [21] Rees JH, Smith SJ, Kullman DM, Hirsch NP, Howard RS. Creutzfeldt-Jakob disease presenting as complex partial status epilepticus: a report of two cases. J Neurol Neurosurg Psychiatry 1999;66:406–13. [22] Fahn S. Phenomenology of movement disorders. In: Fahn S, Marsden CD, Jankovic J, editors. Seventh annual course: a comprehensive review of movement disorders for the clinical practitioner. New York: Columbia University; 1997. p. 3–61. [23] The revision of the surveillance case definition for variant CreutzfeldtJakob disease (vCJD). [WHO/CDS/CSR/EPH/2001.5]. Geneva, Switzerland: World Health Organization; 2001. [24] Hellmann MA, Melamed E. Focal dystonia as the presenting sign in Creutzfeldt-Jakob disease. Mov Disord 2002;17:1097–8. [25] Roos R, Gajdusek DC, Gibbs CJ. The clinical characteristics of transmissible Creutzfeldt-Jakob disease. Brain 1974;96:1–20. [26] Scully RE, Mauk E, McNeely BV. Case records of the Massachusetts General Hospital. N Engl J Med 1983;309:1440–9.
[27] Inzelberg R, Nisipeanu P, Blumen SC, Carasso RL. Alien hand sign in Creutzfeldt-Jakob disease. J Neurol Neurosurg Psychiatry 2000;68: 103–4. [28] Kaneko A, Takei K, Enomoto K, Mitsui T, Nomura K, Iwasaki S, Maruki T, Shimazu K. A case of Creutzfeldt-Jakob disease exhibiting athetosis in the early stage. No To Shinkei 1999;51:887–90. [29] Malteˆte D, Guyant-Mare´chal L, Ge´rardin E, Laquerrie`re A, Martinaud O, Mihout B, Hannequin D. Hemidystonia as initial manifestation of sporadic Creutzfeldt-Jakob disease. Eur J Neurol; in press. [30] Zochodne DW, Young GB, McLachlan RS, Gilbert JJ, Vinters HV, Kaufmann JCE. Creutzfeldt-Jakob disease without periodic sharp wave complexes. Neurology 1988;38:1056–60. [31] Bowen J, Mitchell T, Pearce R, Quinn N. Chorea in new variant Creutzfeldt-Jakob disease. Mov Disord 2000;15:1284–5. [32] McKee D, Talbot P. Chorea as a presenting feature of variant Creutzfeldt-Jakob disease. Mov Disord 2003;18:837–8. [33] Iida T, Doh-Ura K, Kawashima T, Abe H, Iwaki T. An atypical case of sporadic Creutzfeldt-Jakob disease with Parkinson’s disease. Neuropathology 2001;21:294–7. [34] Levine DN. The alien hand. In: Joseph AB, Young RR, editors. Movement disorder in neurology and neuropsychiatry. Oxford: Blackwell; 1999. p. 645–9. [35] Litvan I, Agid Y, Calne D, Goetz C, Jankovic J, Wenning GK, Lai EC, Verny M, Ray-Chaudhuri K, McKee A, Jellinger K, Pearce RK, Bartko JJ. Accuracy of the clinical diagnosis of corticobasal degeneration: a clinicopathologic study. Neurology 1997;48:119–25. [36] Mahapatra RK, Edwards MJ, Schott JM, Bhatia KP. Corticobasal degeneration. Lancet Neurol 2004;3:736–43. [37] Josephs KA, Tang-Wai DF, Edland SD, Knopman DS, Dickson DW, Parisi JE, Petersen RC, Jack CR, Boeve BF. Correlation between antemortem magnetic resonance imaging findings and pathologically confirmed corticobasal degeneration. Arch Neurol 2004;61:1881–4. [38] Cannard KR, Galves-Jimenez N, Watts RL. Creutzfeldt-Jakob disease presenting and evolving as rapidly progressive corticobasal degeneration. Neurology 1998;50:A95–6. [39] Deramecourt V, Girard-Buttaz I, Verier A. A case of spongiform encephalopathy mimicking cortico-basal degeneration. Rev Neurol 2004;160:592–4. [40] Kleiner-Fisman G, Bergeron C, Lang AE. Presentation of CreutzfeldtJakob disease as acute coticobasal degeneration syndrome. Mov Disord 2004;19:948–9. [41] Kovacs GG, Trabattoni G, Hainfellner JA, Ironside JW, Knight RS, Budka H. Mutations of the prion protein gene phenotypic spectrum. J Neurol 2002;249:1567–82. [42] Oberndorfer S, Urbanits S, Lahrmann H, Jarius C, Albrecht G, Grisold W. Familial Creutzfeldt-Jakob disease initially presenting with alien hand syndrome. J Neurol 2002;249:631–2. [43] Litvan I, Agid Y, Calne D, Campbell G, Dubois B, Duvoisin RC, Goetz CG, Golbe LI, Grafman J, Growdon JH, Hallett M, Jankovic J, Quinn NP, Tolosa E, Zee DS. 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. [44] Bertoni JM, Label LS, Sackelleres JC, Hicks SP. Supranuclear gaze palsy in familial Creutzfeldt-Jakob disease. Arch Neurol 1983;40: 618–22. [45] Bertoni JM, Brown P, Goldfarb LG, Rubenstein R, Gajdusek DC. Familial Creutzfeldt-Jakob disease (codon 200 mutation) with supranuclear palsy. JAMA 1992;268:2413–5. [46] Kawasaki K, Wakabayashi K, Kawakami A, Higuchi M, Kitamoto T, Tsuji S, Takabashi H. Thalamic form of Creutzfeldt-Jakob disease or fatal insomnia? Report of sporadic case with normal prion protein genotype Acta Neuropathol 1997;93:317–22. [47] Shimamura M, Uyama E, Hirano T, Murakami T, Mita S, Kitamoto T, Uchino M. A unique case of sporadic Creutzfeldt-Jakob disease presenting as progressive supranuclear palsy. Intern Med 2003;42: 195–8.
D. Malteˆte et al. / Parkinsonism and Related Disorders 12 (2006) 65–71 [48] Josephs KA, Tsuboi Y, Dickson DW. Creutzfeldt-Jakob disease presenting as progressive supranuclear palsy. Eur J Neurol 2004;11: 343–6. [49] Nitrini R, Teixeira da Silva LS, Rosemberg S, Caramelli P, Mestrinelli Carrilho PE, Lughetti P, Passos-Bueno MR, Zatz M, Albrecht S, LeBlanc A. Prion disease resembling frontotemporal dementia and parkinsonism linked to chromosome 17. Arq Neuropsiquiatr 2001;59:161–4. [50] Foster NL, Wilhelmsen K, Sima AA, Jones MZ, D’Amato CJ, Gilman S. Frontotemporal dementia and parkinsonism linked to chromosome 17: a consensus conference. Ann Neurol 1997;41: 706–15. [51] Collie DA, Summers DM, Sellar RJ, Ironside JW, Cooper S, Zeidler M, Knight R, Will RG. Diagnosing variant CreutzfeldtJakob disease with the pulvinar sign: MR imaging findings in 86 neuropathologically confirmed cases. Am J Neuroradiol 2003;24: 1560–9. [52] Zeidler M, Sellar RJ, Collie DA, Knight R, Stewart G, Macleod MA, Ironside JW, Cousens S, Colchester AC, Hadley DM, Will RG. The pulvinar sign on magnetic resonance imaging in variant creutzfeldtJakob disease. Lancet 2000;355:1412–8. [53] Cambier DM, Kantarci K, Worrell GA, Westmoreland BF, Aksamit AJ. Lateralized and focal clinical, EEG, and FLAIR MRI abnormalities in Creutzfeldt-Jakob disease. Clin Neurophysiol 2003; 114:1724–8. [54] Lee MS, Marsden CD. Movement disorders following lesions of the thalamus or subthalamic region. Mov Disord 1994;9:493–507. [55] Bhatia KP, Marsden CD. Behavioral and motor consequences of focal lesions of the basal ganglia in man. Brain 1994;117:859–79. [56] Guentchev M, Groschup MH, Kordek R, Liberski PP, Budka H. Severe, early and selective loss if subpopulation of GABAergic inhibitory neurons in experimental transmissible spongiform encephalopathies. Brain Pathol 1998;8:615–23. [57] Belichenko PV, Miklossy J, Belser B, Budka H, Celio MR. Early destruction of the extracellular matrix around parvalbumin-immunoreactive interneurons in Creutzfeldt-Jakob disease. Neurobiol Dis 1999;6:269–79.
71
[58] Au WJ, Gabor AJ, Vijayan N, Markand ON. Periodic lateralized epileptiform complexes in Creutzfeldt-Jakob disease. Neurology 1980;30:611–7. [59] Shibasaki H, Motomura S, Yamashita Y, Shii H, Kuroiwa Y. Periodic synchronous discharge and myoclonus in Creutzfeldt-Jakob disease: diagnostic application of jerk-locked averaging method. Ann Neurol 1981;9:150–6. [60] Steinhoff BJ, Zerr I, Glatting M, Schulz-Schaeffer W, Poser S. Diagnostic value of periodic complexes in Creutzfeldt-Jakob disease. Ann Neurol 2004;56:702–8. [61] Tschampa HJ, Herms JW, Schulz-Schaeffer WJ, Maruschak B, Windl O, Jastrow U, Zerr I, Steinhoff BJ, Poser S, Kretschmar HA. Clinical findings in sporadic Creutzfeldt-Jakob disease correlate with thalamic pathology. Brain 2002;125:2558–66. [62] Gatto EM, Zurru MC, Rugilo C, Mitre S, Pardal AM, Martinez M, Pardal MM. Focal myoclonus associated with posterior thalamic hematoma. Mov Disord 1998;13:182–4. [63] Marsden CD, Obeso JA, Zarrang JJ, Lang AE. The anatomical basis of symptomatic hemidystonia. Brain 1985;108:463–83. [64] Lehe´ricy S, Vidailhet M, Dormont D, Piero L, Chiras J, Mazetti P, Marsault C, Agid Y. Sriatopallidal and thalamic dystonia: an MR anatomoclinical study. Arch Neurol 1996;53:241–50. [65] Kim JS. Delayed onset mixed involuntary movements after thalamic stroke. Clinical, radiological and pathophysiological findings. Brain 2001;124:299–309. [66] Dietl T, Auer DP, Modell S, Lechner C, Trenkwalder C. Involuntary vocalisations and complex hyperkinetic movement disorder following left side thalamic haemorrhage. Behav Neurol 2003;14:99–102. [67] Sharp FR, Rando TA, Greenberg SA, Brown L, Sagar SM. Pseudochoreoathetosis. Movements associated with loss of proprioception. Arch Neurol 1994;51:1103–9. [68] Feinberg TE, Schindler RJ, Flanagan NG, Haber LD. Two alien hand syndromes. Neurology 1992;42:19–24. [69] Soler R, Vivancos F, Munoz-Torrero JJ, Arpa J, Barreiro P. Postural tremor after thalamic infarction. Eur Neurol 1999;42:180–1. [70] Todd NV, Morrow J, Doh-ura K, Dealler S, O’Hare S, Farling P, Duddy M, Rainov NG. Cerebroventricular infusion of pentosan polysulfate in human variant Creutzfeldt-Jakob disease. J Infect 2005; 50:394–6.