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Hyperkinetic movement disorders during and after acute stroke: The Lausanne Stroke Registry
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NEUROLOGICAL SCIENCES Journal of the Neurological Sciences 146 (1997) 109-116
Hyperkineticmovementdisorders during and after acute stroke: The Lausanne Stroke Registry F. Ghika-Schmid, J. Ghika *, F. Regli, J. Bogousslavsky Department of Neurology, Centre Hospitalier Uniuersitaire Vaadois, CHUV-BH 13, 1011 Luusanne, Switzerland Received 21 March1996;revised 16 July 1996;accepted8 August1996
Abstract Background and objective: To study consecutive patients with acute or delayed hyperkinetic movement disorders in the Lausanne Stroke Registry. Methods: We have identified 29 patients with acute or delayed movement disorders among 2500 patients who had their first-ever acute stroke in the Lausanne Stroke Registry. Serting: Department of Neurology, Lausanne University Hospital. Results: Our
patients presented with hemichorea–hemibaliism(11 patients), hemidystonia(5 patients), stereotypias (2 patients), jerky dystonic unsteadyhand (3 patients),asterixis(2 patients),initial limb-shaking(2 patients),bilateraltremor(1 patients),bilateraljaw myoclonus(1 patient),hemiakathisia(1 patient)and dysarthria-dyskinetichand (1 patient).On neuroimaginga lesion was found in 25 of the 29 cases in the territoryof the middlecerebralartery(7 deep, 2 superficial and 2 complete), the posterior cerebral artery (1 1 patients), both middle and posterior cerebral arteries (2 patients) or the anterior cerebral artery ( 1 patient). The jerky dystonic unsteady hand syndrome was associated with a specific lesion, an infarct in the territory of the posterior choroidal artery. Presumed small-vessel disease was the commonest cause of stroke (15 patients). Only 3 patients had persistent movements ( >6 months). Conclusion: Hyperkinetic movement disorders are uncommon in acute stroke (lYo), the commonest types being hemichorea–hemiballism and hemidystonia. These movement disorders are associated with stroke involving the basal ganglia and adjacent white matter in the territory of the middle or the posterior cerebral artery. The jerky dystonic unsteady hand syndrome is specifically associated with a small infarct in the territory of the posterior choroidal artery. The abnormal movements usually regress spontaneously. 0 1997 Elsevier Science B.V. All rights reserved. Keyword~: Stroke; Movement disorders; Hemichorea–hemiballism; Dystonia
1. Introduction Acute, paroxysmal, recurrent, transient, permanent and delayed abnormal movements have been reported in stroke. Most of these reports are isolated and a survey based on a huge series of patients with movement disorders associated with stroke has been only reported recently (D’Olhaberriague et al., 1995). We here report the prevalence and clinical features of abnormal movements in patients admitted consecutively to the Lausanne Stroke Registry (LSR) Bogousslavsky et al., 1988b over 14 years.
2. Methods We retrospectively reviewed all those patients included into the LSR (Bogousslavsky et al., 1988b) who developed
‘ Corresponding author. Tel.: + 41-21-3141246; fax: + 41-21-3145520. 0022-510X/97/$17 .00 Cl 1997 Ekevier Science B.V. A1lrights reserved. PII S0022-5 10 X(96) O0290-O
hyperkinetic movement disorders during, or after acute stroke and patients who attended our Movement Disorders Unit or the outpatient facility of our hospital for delayed hyperkinetic movement disorders related to a previous cerebrovascular event. Not all patients with a previous acute stroke or hemorrhage had systematic follow-up in our outpatient unit, and therefore the prevalence of delayed hyperkinetic syndromes may be underestimated. All patients were examined by at least one senior investigator from the stroke unit (JB, FR, JG) and one senior member of the Movement Disorder Program (JG). When accepted by the patients, videotape recording was performed and surface EMG were performed in all patients seen after 1991. They underwent the standard LSR investigations, including CT (or MRI from 1989) scans, Doppler ultrasound, ECG, blood tests; angiography and echocardiography were performed on selected cases. 80% of the patients were examined within 24 h of stroke onset and 10070 within 5 days. The protocol of the LSR has been detailed elsewhere (Bogousslavsky et al., 1988b).
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Patients were classified by the features of the abnormal hyperkinetic movement disorders, excluding seizures and hypokinetic syndromes such as parkinsonism or akinetic mutism, according to the generally accepted definitions (Adamsand Victor, 1993; Kase et al., 1981; Dewey and Jankovic, 1989; Garcin, 1955; Demierre and Rondot, 1983; Levis and Russo, 1983; Marsden et al., 1985; Young et al., 1976; Degos et al., 1979; Morrey et al., 1979; Shuttleworth and Drake, 1987; Tarsy et al., 1977; Baquis et al., 1985; Fisher, 1962; Hess et al., 1991; Margolin and Marsden, 1982; Michel et al., 1989; Yanagihara et al., 1985; Avanzani et al., 1977; Sutton and Mayer, 1974; Kim, 1992; Ghika and Bogousslavsy, 1995; Bhatia and Marsden, 1994; Maranganore et al., 1991; Ghika et al., 1995a; Nadeau et al., 1994; Ghika et al., 1994; Ghika et al., 1995b; Louis et al., 1996): hemichorea–hemiballism (Garcin, 1955; Kase et al., 1981; Dewey and Jankovic, 1989; Vidakovic et al., 1994): variable mixture of hemiballism (explosive, very fast, large amplitude involuntary, arrhythmia, mostly proximal movements on one side of the body occurring at rest but increased on action), hemichoreo–athetosis (rapid involuntary movements of one side of the body, with flexion–extension, rotation or crossing movements with distal predominance), some degree of dystonia, often present being admitted; focal, segmental or hemidystonia: (Garcin, 1955; Demierre and Rondot, 1983, Levis and Russo, 1983; Marsden et al., 1985) persistent inappropriate posture at rest or on action, in overfIexion, overextension, or rotation; unilateral asferixis; (Young et al., 1976; Degos et al., 1979; Morrey et al., 1979; Shuttleworth and Drake, 1987; Tarsy et al., 1977) failure to sustain muscle contraction during postures, with intermittent, generally arrhythmia, lapses in muscle tone, essentially found in hand or foot; limb shaking (Baquis et al., 1985; Fisher, 1962; Hess et al., 1991; Margolin and Marsden, 1982; Michel et al., 1989; Yanagihara et al., 1985) involuntary uncontrollable coarse, irregular shaking, wavering, flapping, circling or trembling of a limb, often in orthostatic condition; focal myoclonus: (Avanzani et al., 1977; Sutton and Mayer, 1974 any brief muscle jerk present at rest, in reaction to stimuli, or during action; focal or hemi-tremor (Kim, 1992): regular sinusoidal oscillatory movement centered by a joint); we chose to use a strictly descriptive terminology for other clinical presentations not fitting theses classical subtypes, stereotypic: (Ferbert et al., 1990; Maranganore et al., 1991; Bhatia and Marsden, 1994; Ghika and Bogousslavsy, 1995; Ghika et al., 1995b) simple or complex apparently normal, but involuntary and repetitive stereotyped movements; apraxia (Nadeau et al., 1994) was not included; we already defined in a previous report (Ghika et al., 1994) the jerky dystonic unsteady hand, which was the shortest appellation we could find in order to describe a highly complex delayed hyperkinetic syndrome associating various degree of atheto-choreo-ballic features with dystonia, myoclonus, cerebella outflow myoclonus with inability to keep the hand steady; hemi-
akathisia (Ghika et al., 1995a), which was also previously described as an irresistible feeling of an urge to move one hemibody associated with stereotyped wiggling of the fingers and toes, flexions and extensions of leg and unilateral pacing of the leg; we called the dysarthria and dyskinetic hand a hyperkinetic movement disorder, which has not been previously described, associating an acute dysarthria with stereotyped wiggling of the ipsilateral fingers. Lesions were localized by either CT or MRI in each patient according to our templates of the vascular territories of the deep perforators from the middle cerebral artery (MCA) (Ghika et al., 1989) and posterior cerebral artery PCA (Bogousslavsky et al., 1988a).
3. Results We identified 15 women (mean age 73 years, range 60-90) and 14 men (mean age 67 years, range 32-84) among 2500 first stroke patients. The abnormal movements occurred on the right side in 16 patients, on the left side in 11, and on both sides in 2. On neuroimaging a focal lesion was found in 25 cases (86%). One patient had diffuse leukoaraiosis. No lesions were detected in 3 patients who only had CT, while all patients who had MRI showed a visible lesion. Two patients had a hemorrhage, 1 had a hemorrhagic infarct and 22 had an infarct. Fifteen patients had a small infarct ( <1.5 mm) and ten had a large lesion (ischemic or hemorrhagic). The clinical and radiological characteristics are summarized in Table 1. 3.1. Abnormal movement subtypes The majority of our patients presented with hemichorea–hemiballism (1 1 cases); some degree of dystonia or athetosis was constantly found (Table 1). Pure hemiballism was found in 3 patients (patients 4, 5 and 6), with lesions found respectively in the thalamus, parieto-occipital and internal capsule regions, and internal capsule plus lenticulate nucleus. Hemichoreo-athetosis was found in 3 patients (1, 2 and 3), with no lesion seen on CT (MRI was not available) in one patient, and in the thalamus in the other two ones. Hemichoreo–ballism was found in 3 patients (9, 10 and 11) with no lesion but leukoaraiosis in the first one, an old caudate infarct in the second, and a caudate and lenticular infarct in the third one. Hemichorea–hemiballism was the most frequent presentation (38%) of hyperkinetic movement disorders in our registry (prevalence 0.4%). Hemiparesis was associated in all but one patient, three also had a hemisensory deficit, and ataxia was found in one patient. On CT, there were 9 infarcts and 1 hemorrhage and 1 case without visible lesion. Lesions were located in the territory of the deep perforators from the posterior cerebral artery and the middle cerebral artery (lateral Ienticulosatriate and anterior
F. Ghika-Schmid et al./Jourruzl of the Neurological Sciences 146 (1997) 109-II6
choroidal arteries). None of these additional signs could be used to localise the lesion within the basal ganglia. Pure choreo–ballism without associated signs was present in only one patient, who had a striatal infarct. The symptoms were transient in 6 patients (after haloperidol in 4). Some degree of choreo-ballism was found in the jerky dystonic unsteady hand (see after) with infarcts in the territory of the posterior choroidal artery. Dystonia (5 cases) was the second most frequent presentation (17%). A persistent focal or segmental dystonic posture of the hand (also known as thalamic hand) (patient 15), or involving the entire upper extremity (segmental dystonia) (patients 16 and 17) or hemidystonia (patients 18 and 19) was found in all but one patient had transient symptoms (patient 17). In three patients, the lesion was located in the territory of the deep perforators from the PCA territory, involving the thalamus, and in two cases the lesion was in the striatum, (i.e. in the territory of the lenticulostriate arteries (LS) from MCA). In two patients, there was a superficial MCA infarct in the sub-cortical white matter of the frontal and parietal lobes. All had associated hemiparesis, but no sensory deficit. No associated neurological dysfunction was of use in localizing the lesion. No patient had painful tonic spasms or generalized
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dystonia. Some dystonic postures were found in association with hemichorea–hemiballism or jerky dystonic unsteady hand. Stereotypias (2 cases) were found in patients 12 and 13, one with left MCA and a lateral lenticulostriate territory infarct and one with parietal infarct. Patient 12 showed transient localized rapid, non clonic, apparently normal but involuntary movement of the right eyelid and hand, followed by progressive right hemiparesis, hemihypesthesia and global aphasia, associated with left occlusion of the internal carotid artery on angiography. A third patient (patient 29) had acute dysarthria associated with repetitive wiggling movement of the fingers. On MRI a lenticulostriate infarct was found. This clinical picture has not been previously reported and we called it ‘dysarthria and dyskinetic hand’, because this could be another lacunar syndrome. All 3 patients had sensory-motor deficits and one patient had aphasia related to a LS infarct. No clear anatomical correlation could be made. Three patients with an unusually, highly complex, delayed hyperkinetic syndrome, which we described elsewhere as the jerky dystonic unsteady hand (patients 20, 21 and 22) had an infarct in the posterior thalamic nuclei (in the territory of the posterior choroidal artery). The syn-
Table 1 Clinical presentation and neuroimaging Case
Clinical presentation
Neuroimaging
Arterial territory involved
.I .nemlcnorea–nemmamsrn . , ., .<.
2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27
CT: no visible lesion CT: r thalamic infarct I hemichorea–hemiballism CT: 1thalamic Iacunar infarct r hemichorea–hemiballism CT: 1parieto occipital and internal capsule hemon’hage r hemichorea–hemiballism CT: leukoaraiosis, 1post capsular infarct r hemichorea–hemiballism CT: left capsulolenticular infarct, Ierrkoencephalopathy r hemichorea–hemiballism CT: I sub-thakunic infarct r hemichorea–hemiballism CT: superficial and deep I MCA infarct r hemichorea–hemiballism CT: r white matter infarct 1hemichorea–hemiballism CT: r old infarct of the head of the caudate, no new lesion r hemichorea–hemiballism CT: 1subacute Ienticular and head of the caudate infarcts r hemichorea–hemiballism CT: 1caudo-putamen and irrtemal capsule infarcts r stereotypic CT: post superficial infarct in the right MCA territory 1stereotypic CT: Ieukoaraiosis, no other visible lesion bilateral jaw myodonia CT: 1subacute frontal parasagittal infarct r hand dystonia and rigidity MRI: I ant / r post fhalamic, pontine, 1cerebella infarcts 1segmental dystonia CT: 1post capsulolenticular infarct r segmental dystonia CT: 1thalamic hemorrhage, 1capsulolenticular infiirct 1hemidystonia CT: 1parieto-tcmporal hemorrhagic infarct r hemidystonia CT: I occipito-temporal, cerebella, 1thalamic infarcts r jerky dystonic unsteady hand MR1: old I pulvinar and lingual gyms infarcts r jerky dystonic unsteady hand CT: r thalamic infarct 1jerky dystonic unsteady hand inaugural 1limb shaking CT: no visible lesion CT: r post borderzone infarct inaugural 1 limb shaking bilateral tremor preceding stroke MRI: bilateral (r > 1)pontine infarct CT: acute r capsulo-thalamic hematoma I astenxis MRI: 1ant paramedian thalamic, r and I cerebella infarcts r astenxis
28 29
r hemiakathisia 1dysartfria and dyskinetic hand
1
MR1: I post thalamic infarct CT: no visible lesion
r PCA: thakrmoperforating, TGA I PCA 1MCA 1PCA: post choroidal 1MCA (LLS) 1PCA 1MCA r McA (LLS) r MCA I MCA (LLS) I McA (LLS) r MCA 1ACA 1PCA I MCA (LLS)) 1PCA+MCA (LLS) 1MCA 1PCA: post choroidal 1PCA: post choroidal r PCA: post cboroidal I MCA (CBF decreased perfusion) r MCA + PCA basilar r PCA 1PCA: tubero-tfralamic, post inf cerebella 1PCA: post choroidal
U: upper extremity; L: lower extremity; F: face; 1:left; r: right; ant: anterior; post: posterior; PCA: posterior cerebral artery; MCA: middle cerebral artery; LLS: lateral lenticulostriate artery; TGA: thalomogeniculate artery; CBF: cerebral blood flow.
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I I
Fig. 1. Summary of the lesions seen in: 1.I and 1.2 hemichorea–hemiballism (1 1 cases); 1.3 and 1.4 hemidystonia (5 cases); 1.5 dyskinesia (2 cases); 1.6 jerky dystonic unsteady hand (3 cases); 1.7 asterixis (2 cases); 1.8 limb-shaking (2 cases).
drome, developed 12 to 18 weeks after the acute stroke in the posterior cerebral artery, which was accompanied by a painful thalamic D6jerine-Roussy syndrome; the delayed hyperkinetic syndromes were characterized by an intense hyperkinetic choreo-atheto-ballic syndrome, together with dystonic posture of the hand and myoclonic-ataxic movements in patients 21 and 22. Patient 20 had right hyperpathia and right hand dystonia with athetosis of the fingers, ataxia and cerebella outflow ‘rubral’ tremor. Limb-shaking (N= 3) in patient 23 was characterized
I
1 Fig. 1 (continued).
1 Fig. 1 (continued),
by a transient brisk arrhythmia shaking of the right arm associated with amaurosis in the left eye in recurring episodes each lasting 2 to 10 rein, which lasted for 3 weeks. Angiography showed left internal carotid occhtsion. On CT, no lesion was visible. On EEG, rare left anterior theta element bursts, were present. SPECT showed a slightly decreased perfusion of the left MCA territory. The hypothesis of repeated transient hemodynamic isI
1
1 . Fig. I (continued).
F. Ghika-Schmid et al./Journal of the Neurological Sciences 146 (1997) 109–116
chemia in the deep left MCA territory was raised. Patient 24 had initial left upper limb-shaking, followed by left facial weakness, visual agnosia and a transient episode of visual hallucination. On CT, a right posterior watershed infarct was found. Thus, initial limb shaking was found in three patients, one with decreased regional cerebral blood flow in the MCA territory, one with posterior watershed infarct, and the third with pontine ischemic lesion. In all three patients this was associated with hemiparesis. The movements were more prominent on the arm than the leg. Two patients had an internal carotid artery stenosis. Patient 25 had intermittent bilateral tremor in the upper extremities preceding a tetraparesis with left hemianesthesia, corticobulbar signs and dysarthria. On MRI, a right paramedian pontic infarct was found in the territory of the paramedian perforating branches of the basilar artery. Focal unilateral asterixis was found in two patients. Patients 26 and 27 had unilateral upper extremity asterixis which occurred in the acute phase of stroke. In the first patient, a sensory-motor hemiparesis was associated and an acute capsular-thalamic hemorrhage was seen on CT, whereas in the second patient hemiparesis only was found on examination and a paramedian thalamic infarct in the territory of the tubero-thalamic artery, together with bilateral hemispheric cerebella infarcts were found on MRI. We found focal action myoclonus of the jaw and tongue in one patient (patient 14) with diffuse leukoaraiosis. The abnormal bilateral myoclonus occurred only when the patient tried to speak, without palatal myoclonus, but with dysarthria, bucco-linguo-facial apraxia, bilateral facial weakness, and hemiparesis involving the right arm. This clinical picture has not previously been reported. The three patients with the jerky unsteady hand syndrome had some degree of action myoclonus. Transient delayed hemiakathisia (N= 1) was found in one patient (patient 28), who presented an acute right hand and foot sensory loss involving all modalities and mild right cortico-spinal signs. On MRI a small infarct was found in the posterior thalamic nuclei involving the pulvinar, probably in the territory of the lateral branches of the left posterior choroidal artery. Five months later he developed kinesiogenic pain on the same side, with features of a D6jerine-Roussy syndrome, which evolved in a few weeks toward a painless urge to move associated with stereotyped movements of the right hemibody (hemiakathisia). The patients with the jerky dystonic unsteady hand syndrome had some feature of restlessness of the hand, which was unable to be kept steady, but no feeling of an urge to move. The summary of the topography of lesions according to the described hyperkinetic syndromes are summarized on Fig. 1. 3.2. Evolution Evolution. All but 4 patients presented acute onset movement disorders concomitant with other deficits. The 4
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patients with delayed syndromes attended the outpatient unit because of the hyperkinesia, but none was expected to occur. The length of the follow-up ranged from 1 week in cases of early regression to 5 years in cases of persistent symptoms. Seven patients were lost from FU. Eleven of 19 untreated patients showed spontaneous regression within 2 weeks. Five patients with hemichorea–hemiballism were treated with haloperidol (doses 1.5 to 9 mg/day) with complete regression within a week, 5 had spontaneous remission without treatment, and one had persistent symptoms. Among the 5 patients with dystonia, only one received clonazepam, with regression within a week, three patients received no treatment, among them two were lost for follow-up and one kept some dystonia of the hand. None of the 3 patients with the jerky dystonic unsteady hand responded to any medication. The hemiakathisia disappeared after a week of clonazepam, and the dysarthria and dyskinetic hand regressed spontaneously without treatment. Six patients showed persistent movement disorder and were unresponsive to all treatment (patients 11, 15, 20, 21, 22 and 23). No patient had recurrent hyperkinetic movement disorders.
4. Discussion Hyperkinetic movement disorders are uncommon in acute stroke, with a prevalence of 29/2500 (1%) and an estimated incidence of 0.08% per year in our hospital-based study. Over the studied period, the total number of patients with subcortical ischemic or hemorrhagic involvement of a large portion of the basal ganglia without causing movement disorders was 536 out of 2500 strokes of any etiology. This observation underlines the rare occurrence of movement disorders in the acute phase of stroke, despite the frequent involvement of the basal ganglia, and could suggest the possibility of strategic locations within the basal ganglia for movement disorders to occur, or peculiar personal idiosyncrasy or features of brain plasticity within these anatomical networks. It is, however, possible that our figures have been underestimated because of the intermittent, transient, spontaneously regressive or delayed nature of their presentation and often the patients or even their family deny that the symptoms were present. The retrospective nature of this study may also lead to an underestimation of prevalence. Indeed in our patients, referred for stroke, the movement disorder was a prominent feature, which resulted in the subsequent examination by a movement disorder specialist, but non obvious presentations of movement disorders may easily escape the attention of non specialists in the field. For these reasons, and because of the large number of patients who were lost for follow up in our outpatient unit after their vascular event, the prevalence of delayed movement disorders cannot be correctly assessed in this study. A lesion involving the basal ganglia (pallidum, puta-
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men, caudate, thalamus) was found in all our cases examined with MRI, whereas the two patients without visible lesion, or the other two ones with lesions involving the hemispherical white matter alone had only CT. These observations suggest that basal ganglia involvement may be critical, although the small number of cases does not allow to rule out the possibility that movement disorders can also occur with superficial lesions not involving the basal ganglia (Ferbert et al., 1990; Shintani et al., 1991; Takeshita et al., 1993). However, this has to be interpreted with caution, because of the small number of MRI scans in our patients. Among basal ganglia, the striatum and pallidum were most frequently involved (44%) (i.e. the territory of the lateral lenticulo-striate arteries), followed by the thalamus (lateral and posterior nuclei) (37Yo)and the subthalamic nucleus (1 case). This observation supports the concept of a global functional network within the basal ganglia (Ghika and Bogousslavsy, 1995; Bhatia and Marsden, 1994) with the interruption of either the direct or the indirect pathway in the basal ganglia by focal lesion. It refutes any clear specificity of the subthalamic nucleus for hemichorea–hemiballism, of the caudate for choreo– athetosis, and of the putamen or globus pallidus for hemidystonia, as already reported (Martin, 1957; Papez et al., 1942; Critchley, 1953; Buruma et al., 1986; Zeman and Whitlock, 1968; Pettigrew and Jankovic, 1985; Burke et al. 1980; L4hercy et al., 1996; Lee and Marsden, 1994; Peterson and Peterson, 1987) and this is in accord with recent studies (D’Olhaberriague et al., 1995; Ghika and Bogousslavsy, 1995; Martin, 1957; LEhercy et al., 1996; Lee and Marsden, 1994; Johnson and Fahn, 1977; Bhatia et al., 1994). As mentioned in these studies, lesions responsible for hemichorea–hemiballism were found in the subthalamic nucleus, but were also found in the thalamus, the pathways interconnecting these nuclei (i.e. in the territory of the perforators of the PCA), the striatum (caudate– putamen) and the pallidum (i.e. in the territory of the deep perforators from the MCA), without involvement of the subthalamic nucleus. ~Similarly, in patients with dystonia, the lesion was located in the territory of the deep perforators from the PCA territory, involving the thalamus, and in two cases the lesion was in the striatum, (i.e. in the territory of the lenticulostriate arteries (LS) from MCA), as previously reported (D’Olhaberriague et al., 1995; Levis and Russo, 1983; Marsden et al., 1985; Ghika and Bogousslavsy, 1995; Martin, 1957; L6hercy et al., 1996; Lee and Marsden, 1994). In the same direction, unilateral asterixis has been reported with infarct in the contralateral fronto– parietal cortex, basal ganglia, cerebellum, thalamus, or brainstem (Young et al., 1976; Degos et al., 1979; Morrey et al., 1979; Shuttleworth and Drake, 1987; Tarsy et al., 1977; Peterson and Peterson, 1987; Bril et al., 1979), which confirms the non-specific nature of asterixis, which can be found with lesions of the sensory-motor system network. The prevalence of unilateral asterixis is probably largely underestimated and has to be looked for and recog-
nized in the acute phase of stroke. Other types of myoclonus found in association with vascular lesions are not specific for any location either. A patient with intention and action myoclonus had a thalamic angioma (Avanzani et al., 1977) and ‘focal reflex myoclonus’ has been reported in a patient with a superficial MCA stroke (Sutton and Mayer, 1974). We found focal action myoclonus of the tongue in only one patient (case 14); this confirms that non epileptic myoclonus seems to be very rare in stroke, and non specific for any topographical location. Tremor was the only movement disorder that we found with a brainstem infarct, but dystonia and asterixis have also been reported in brainstem lesions (Morrey et al., 1979; Baquis et al., 1985; Peterson and Peterson, 1987; Bril et al., 1979). Acute contralateral or ipsilateral stereotypias (Maranganore et al., 1991; Ghika et al., 1995b) had no specificity for any anatomical location. The ‘jerky dystonic unsteady hand syndrome’ (Ghika et al., 1994) is the only hyperkinetic syndrome which was found to be specific for a topographic localization, i.e the posterior thalamic nuclei in the territory of the posterior choroidal artery. Our findings highlight the many subtypes of simple or complex movement disorders (initial, transient, recurrent or delayed) which can be found in stroke involving the basal ganglia, thalamus, sub-cortical white matter and, more rarely, the brainstem. Delayed, recurrent or paroxysmal hemichorea–hemiballism or generalized ballism or chorea (Johnson and Fahn, 1977) or ataxia (Louis et al., 1996) were not seen, but one patient had transient delayed hemiakathisia and three had the delayed ‘the jerky dystonic unsteady hand’ (Ghika et al., 1995a) occurring weeks to months after the acute lesion. All had thalamic infarcts, and this location seems to be one of the best documented strategic anatomical structures for delayed syndromes to occur. Delayed tremor and dystonia have also been reported with lesions in the thalamic nuclei (Kim, 1992). Hyperkinetic movement disorders in stroke occur mostly unilaterally (83Yo),contralaterally to the lesion. We found bilateral asymmetric ballismus, bilateral tremor and limb shaking, and bilateral jaw and tongue myoclonus in 5 patients (17%). Two patients had bilateral lesions (bilateral pontine infarct, leukoaraiosis), but we did not observe abnormal movement strictly ipsilateral to a brain lesion, as reported by others (Peterson and Peterson, 1987; Bril et al., 1979; Moersh and Kemohan, 1939; Dierssen et al., 1961). The limb shaking ipsilateral to the side of the large vessel stenosis may be due to dysfunction in the ipsilateral cerebella pathways. A releasing role played by the ipsilateral lesion allowing an old silent contralateral lesion to be expressed (Bril et al., 1979), or damage to the connections between the sub-thalamic nucleus on each side (Moersh and Kemohan, 1939) can be postulated in such cases. Two thirds of the lesions were small infarcts ( <1.5 mm), often with leukoaraiosis, which incriminates smallvessel disease as the leading cause of stroke, with hypertension (6590) as the most common risk factor. Large-artery
F. Ghifra-Schmide?al. /Jourrud of the Neurological Sciences J46 (1997) 109-1I6
stenosis was seen with limb shaking, but was otherwise uncommon. As already reported, limb shaking seemed suggestive of hemodynamic problems in the carotid or vertebrobasilar system (Baquis et al., 1985; Fisher, 1962; Hess et al., 1991; Margolin and Marsden, 1982; Yanagihara et al., 1985). Primary hemorrhage was rare. This is in accord with the largest series (D’Olhaberriague et al., 1995). Spontaneous regression of the abnormal movements was seen in half of our patients. Several drugs, including haloperidol, perphenazine, reserpine, tetrabenazine, valproate, chlorpromazine, clonazepam (Adams and Victor, 1993; Dooling and Adams, 1975; Obeso et al., 1984; Milandre et al., 1993; Johnson and Fahn, 1977; Tognetti and Donati, 1986; Bhatia et al., 1994) have been reported to be successful in the treatment of acute hemichorea– hemiballism. Only 3 patients, including 2 with delayed hyperkinetic symptoms resistant to medication, had persistent movement disorders. The nature of this study made it difficult to assess accurately the response to treatment and we will therefore not draw any conclusions from these observations. In conclusion, hyperkinetic movement disorders are infrequent in stroke, but can be found in the acute phase or can be delayed by weeks or months, especially when the lesion in the posterior thalamic nuclei. Generally unilateral, and largely regressive, there may be exceptions to these rules. The clinical pictures are not specific for any anatomical location in a basal ganglia or in the territory of any vessel, except in posterior thalamic nuclei, and this is in accord with the global concept of a complex network with parallel processing in the basal ganglia.
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Martin, J.P. (1957) Hemichorea-(hemiballismus) wittrout lesion in the corpus Luysii. Brain, 80: 1– 10. Michel, B., P. Lemarquis, F. Nicoli and J.L. Gastaut (1989) Movements involontaires positionnels:”accks isch6miques carotidiens. Rev. Neurol., 12: 853–855. Milandre, L., C. Brosset, B. Gabriel and R. Khalil (1993) Movements involontaires transitoires et infarctus thalamiques. Rev. Neurol., 149: 402-406. Moersh, F.P. and J.W. Kemohan (1939) Hemiballismus: a clinicopatJrologic study. Arch. Neurol. Psychiatry, 41: 365–372. Morrey, E.W., J.C. Goodman, T. Stewart and W.L. Bmnnon (1979) Unilateral asterixis: motor integration dysfunction in focal vascular disease. Neurology, 29: 1180-1182. Nadeau, S.E., D.P. Roeltgen, S. Sevush et al. (1994) Apraxia due to pathologically documented thalamic infarction. Neurology, 44: 21332137. Obese, J.A., L.M. Vila, G. Delgado et al. (1984) Delayed onset dystonia following hemiplegic migraine. Headache, 24: 266-268. Papez, J.W., A.E. Benett and P.T. Cash (1942) Hemichorea (hemiballism), association with pallidal lesions involving afferent and efferent connections of subfhalamic nucleus: curare therapy. Arch. Neurol. Psychiatry.,1942; 47: 667–676. Peterson, D.I. and G.W. Peterson (1987) Unilateral asterixis due to ipsilateral lesions in the pens rmdmedulla. Ann. Neurol., 22: 661–663. Pettigrew, L.C. and J. Jankovic (1985) Hemidystonia: A report of 22 patients and review of the literature. J. Neurol. Neurosurg. Psychiatry, 48: 650-657.
Shintani, S., Z. Shiozawa, S. Tsunota and T. Shiigai (1991) Paroxysmal choreoadretosis precipitated by movement, sound and photic stimulation in a case of artenovenous malformation in the parietal lobe. Clin. Neurol. Neurosurg., 93: 237–239. Shuttleworfb, E. and M.E. Drake (1987) Asterixis after lacunar infarctions. Eur. NeuroL, 27: 62–63. Sutton, G.G. and R.F. Mayer (1974) Focal reflex myoclonus. J. Neurol. Neurosurg. Psychiatry, 37: 207-217. Takeshita, I., Y. Hamada and M. Fuktsi (1993) Hemiballistic involuntary movement manifested as a parietal lobe syndrome. Fukuoka Igatiu Zasshi, 84: 374-378. Tarsy, D., B. Lieberman, J. Chirico-Post and F. Benson (1977) Unilateral asterixis associated with a mesencephalic syndrome. Arch. Neurol., 34; 44&447. Tognetti, F. and R. Donati (1986) Hemiballism of ischemic origin: report of a case with unusual anatomical lesion. Acta. Neurol., 8: 150– 153. Vidakovic, A., N. Dragasevic and V.S. Kostic (1994) Hemiballism: report of 25 cases. J. Neurol. Neurosurg. Psychiatry, 57: 945–949. Yanagihara, T., D.G. Piepgras and D.W. Klass (1985) Repetitive involuntary movements associated with episodic cerebral ischemia. Ann. Neurol., 18: 24z-250. Young, R.R., B.T. Shahani and R.N. Kjellberg (1976) Unilateral asterixis produced by discrete central nervous system lesions. Trans. Am. Neurol. Assoc., 101: 306–307. Zeman, W. and C.C. Whitlock (1968) Symptomatic dystonia. In: Vinken P.J. and Bruyn G.W. (Eds.) Handbook of Neurology, Vol. 6. Nocth Holland, Elsevier, pp. 544566.
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NEUROLOGICAL SCIENCES Journal of the Neurological Sciences 146 (1997) 109-116
Hyperkineticmovementdisorders during and after acute stroke: The Lausanne Stroke Registry F. Ghika-Schmid, J. Ghika *, F. Regli, J. Bogousslavsky Department of Neurology, Centre Hospitalier Uniuersitaire Vaadois, CHUV-BH 13, 1011 Luusanne, Switzerland Received 21 March1996;revised 16 July 1996;accepted8 August1996
Abstract Background and objective: To study consecutive patients with acute or delayed hyperkinetic movement disorders in the Lausanne Stroke Registry. Methods: We have identified 29 patients with acute or delayed movement disorders among 2500 patients who had their first-ever acute stroke in the Lausanne Stroke Registry. Serting: Department of Neurology, Lausanne University Hospital. Results: Our
patients presented with hemichorea–hemibaliism(11 patients), hemidystonia(5 patients), stereotypias (2 patients), jerky dystonic unsteadyhand (3 patients),asterixis(2 patients),initial limb-shaking(2 patients),bilateraltremor(1 patients),bilateraljaw myoclonus(1 patient),hemiakathisia(1 patient)and dysarthria-dyskinetichand (1 patient).On neuroimaginga lesion was found in 25 of the 29 cases in the territoryof the middlecerebralartery(7 deep, 2 superficial and 2 complete), the posterior cerebral artery (1 1 patients), both middle and posterior cerebral arteries (2 patients) or the anterior cerebral artery ( 1 patient). The jerky dystonic unsteady hand syndrome was associated with a specific lesion, an infarct in the territory of the posterior choroidal artery. Presumed small-vessel disease was the commonest cause of stroke (15 patients). Only 3 patients had persistent movements ( >6 months). Conclusion: Hyperkinetic movement disorders are uncommon in acute stroke (lYo), the commonest types being hemichorea–hemiballism and hemidystonia. These movement disorders are associated with stroke involving the basal ganglia and adjacent white matter in the territory of the middle or the posterior cerebral artery. The jerky dystonic unsteady hand syndrome is specifically associated with a small infarct in the territory of the posterior choroidal artery. The abnormal movements usually regress spontaneously. 0 1997 Elsevier Science B.V. All rights reserved. Keyword~: Stroke; Movement disorders; Hemichorea–hemiballism; Dystonia
1. Introduction Acute, paroxysmal, recurrent, transient, permanent and delayed abnormal movements have been reported in stroke. Most of these reports are isolated and a survey based on a huge series of patients with movement disorders associated with stroke has been only reported recently (D’Olhaberriague et al., 1995). We here report the prevalence and clinical features of abnormal movements in patients admitted consecutively to the Lausanne Stroke Registry (LSR) Bogousslavsky et al., 1988b over 14 years.
2. Methods We retrospectively reviewed all those patients included into the LSR (Bogousslavsky et al., 1988b) who developed
‘ Corresponding author. Tel.: + 41-21-3141246; fax: + 41-21-3145520. 0022-510X/97/$17 .00 Cl 1997 Ekevier Science B.V. A1lrights reserved. PII S0022-5 10 X(96) O0290-O
hyperkinetic movement disorders during, or after acute stroke and patients who attended our Movement Disorders Unit or the outpatient facility of our hospital for delayed hyperkinetic movement disorders related to a previous cerebrovascular event. Not all patients with a previous acute stroke or hemorrhage had systematic follow-up in our outpatient unit, and therefore the prevalence of delayed hyperkinetic syndromes may be underestimated. All patients were examined by at least one senior investigator from the stroke unit (JB, FR, JG) and one senior member of the Movement Disorder Program (JG). When accepted by the patients, videotape recording was performed and surface EMG were performed in all patients seen after 1991. They underwent the standard LSR investigations, including CT (or MRI from 1989) scans, Doppler ultrasound, ECG, blood tests; angiography and echocardiography were performed on selected cases. 80% of the patients were examined within 24 h of stroke onset and 10070 within 5 days. The protocol of the LSR has been detailed elsewhere (Bogousslavsky et al., 1988b).
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Patients were classified by the features of the abnormal hyperkinetic movement disorders, excluding seizures and hypokinetic syndromes such as parkinsonism or akinetic mutism, according to the generally accepted definitions (Adamsand Victor, 1993; Kase et al., 1981; Dewey and Jankovic, 1989; Garcin, 1955; Demierre and Rondot, 1983; Levis and Russo, 1983; Marsden et al., 1985; Young et al., 1976; Degos et al., 1979; Morrey et al., 1979; Shuttleworth and Drake, 1987; Tarsy et al., 1977; Baquis et al., 1985; Fisher, 1962; Hess et al., 1991; Margolin and Marsden, 1982; Michel et al., 1989; Yanagihara et al., 1985; Avanzani et al., 1977; Sutton and Mayer, 1974; Kim, 1992; Ghika and Bogousslavsy, 1995; Bhatia and Marsden, 1994; Maranganore et al., 1991; Ghika et al., 1995a; Nadeau et al., 1994; Ghika et al., 1994; Ghika et al., 1995b; Louis et al., 1996): hemichorea–hemiballism (Garcin, 1955; Kase et al., 1981; Dewey and Jankovic, 1989; Vidakovic et al., 1994): variable mixture of hemiballism (explosive, very fast, large amplitude involuntary, arrhythmia, mostly proximal movements on one side of the body occurring at rest but increased on action), hemichoreo–athetosis (rapid involuntary movements of one side of the body, with flexion–extension, rotation or crossing movements with distal predominance), some degree of dystonia, often present being admitted; focal, segmental or hemidystonia: (Garcin, 1955; Demierre and Rondot, 1983, Levis and Russo, 1983; Marsden et al., 1985) persistent inappropriate posture at rest or on action, in overfIexion, overextension, or rotation; unilateral asferixis; (Young et al., 1976; Degos et al., 1979; Morrey et al., 1979; Shuttleworth and Drake, 1987; Tarsy et al., 1977) failure to sustain muscle contraction during postures, with intermittent, generally arrhythmia, lapses in muscle tone, essentially found in hand or foot; limb shaking (Baquis et al., 1985; Fisher, 1962; Hess et al., 1991; Margolin and Marsden, 1982; Michel et al., 1989; Yanagihara et al., 1985) involuntary uncontrollable coarse, irregular shaking, wavering, flapping, circling or trembling of a limb, often in orthostatic condition; focal myoclonus: (Avanzani et al., 1977; Sutton and Mayer, 1974 any brief muscle jerk present at rest, in reaction to stimuli, or during action; focal or hemi-tremor (Kim, 1992): regular sinusoidal oscillatory movement centered by a joint); we chose to use a strictly descriptive terminology for other clinical presentations not fitting theses classical subtypes, stereotypic: (Ferbert et al., 1990; Maranganore et al., 1991; Bhatia and Marsden, 1994; Ghika and Bogousslavsy, 1995; Ghika et al., 1995b) simple or complex apparently normal, but involuntary and repetitive stereotyped movements; apraxia (Nadeau et al., 1994) was not included; we already defined in a previous report (Ghika et al., 1994) the jerky dystonic unsteady hand, which was the shortest appellation we could find in order to describe a highly complex delayed hyperkinetic syndrome associating various degree of atheto-choreo-ballic features with dystonia, myoclonus, cerebella outflow myoclonus with inability to keep the hand steady; hemi-
akathisia (Ghika et al., 1995a), which was also previously described as an irresistible feeling of an urge to move one hemibody associated with stereotyped wiggling of the fingers and toes, flexions and extensions of leg and unilateral pacing of the leg; we called the dysarthria and dyskinetic hand a hyperkinetic movement disorder, which has not been previously described, associating an acute dysarthria with stereotyped wiggling of the ipsilateral fingers. Lesions were localized by either CT or MRI in each patient according to our templates of the vascular territories of the deep perforators from the middle cerebral artery (MCA) (Ghika et al., 1989) and posterior cerebral artery PCA (Bogousslavsky et al., 1988a).
3. Results We identified 15 women (mean age 73 years, range 60-90) and 14 men (mean age 67 years, range 32-84) among 2500 first stroke patients. The abnormal movements occurred on the right side in 16 patients, on the left side in 11, and on both sides in 2. On neuroimaging a focal lesion was found in 25 cases (86%). One patient had diffuse leukoaraiosis. No lesions were detected in 3 patients who only had CT, while all patients who had MRI showed a visible lesion. Two patients had a hemorrhage, 1 had a hemorrhagic infarct and 22 had an infarct. Fifteen patients had a small infarct ( <1.5 mm) and ten had a large lesion (ischemic or hemorrhagic). The clinical and radiological characteristics are summarized in Table 1. 3.1. Abnormal movement subtypes The majority of our patients presented with hemichorea–hemiballism (1 1 cases); some degree of dystonia or athetosis was constantly found (Table 1). Pure hemiballism was found in 3 patients (patients 4, 5 and 6), with lesions found respectively in the thalamus, parieto-occipital and internal capsule regions, and internal capsule plus lenticulate nucleus. Hemichoreo-athetosis was found in 3 patients (1, 2 and 3), with no lesion seen on CT (MRI was not available) in one patient, and in the thalamus in the other two ones. Hemichoreo–ballism was found in 3 patients (9, 10 and 11) with no lesion but leukoaraiosis in the first one, an old caudate infarct in the second, and a caudate and lenticular infarct in the third one. Hemichorea–hemiballism was the most frequent presentation (38%) of hyperkinetic movement disorders in our registry (prevalence 0.4%). Hemiparesis was associated in all but one patient, three also had a hemisensory deficit, and ataxia was found in one patient. On CT, there were 9 infarcts and 1 hemorrhage and 1 case without visible lesion. Lesions were located in the territory of the deep perforators from the posterior cerebral artery and the middle cerebral artery (lateral Ienticulosatriate and anterior
F. Ghika-Schmid et al./Jourruzl of the Neurological Sciences 146 (1997) 109-II6
choroidal arteries). None of these additional signs could be used to localise the lesion within the basal ganglia. Pure choreo–ballism without associated signs was present in only one patient, who had a striatal infarct. The symptoms were transient in 6 patients (after haloperidol in 4). Some degree of choreo-ballism was found in the jerky dystonic unsteady hand (see after) with infarcts in the territory of the posterior choroidal artery. Dystonia (5 cases) was the second most frequent presentation (17%). A persistent focal or segmental dystonic posture of the hand (also known as thalamic hand) (patient 15), or involving the entire upper extremity (segmental dystonia) (patients 16 and 17) or hemidystonia (patients 18 and 19) was found in all but one patient had transient symptoms (patient 17). In three patients, the lesion was located in the territory of the deep perforators from the PCA territory, involving the thalamus, and in two cases the lesion was in the striatum, (i.e. in the territory of the lenticulostriate arteries (LS) from MCA). In two patients, there was a superficial MCA infarct in the sub-cortical white matter of the frontal and parietal lobes. All had associated hemiparesis, but no sensory deficit. No associated neurological dysfunction was of use in localizing the lesion. No patient had painful tonic spasms or generalized
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dystonia. Some dystonic postures were found in association with hemichorea–hemiballism or jerky dystonic unsteady hand. Stereotypias (2 cases) were found in patients 12 and 13, one with left MCA and a lateral lenticulostriate territory infarct and one with parietal infarct. Patient 12 showed transient localized rapid, non clonic, apparently normal but involuntary movement of the right eyelid and hand, followed by progressive right hemiparesis, hemihypesthesia and global aphasia, associated with left occlusion of the internal carotid artery on angiography. A third patient (patient 29) had acute dysarthria associated with repetitive wiggling movement of the fingers. On MRI a lenticulostriate infarct was found. This clinical picture has not been previously reported and we called it ‘dysarthria and dyskinetic hand’, because this could be another lacunar syndrome. All 3 patients had sensory-motor deficits and one patient had aphasia related to a LS infarct. No clear anatomical correlation could be made. Three patients with an unusually, highly complex, delayed hyperkinetic syndrome, which we described elsewhere as the jerky dystonic unsteady hand (patients 20, 21 and 22) had an infarct in the posterior thalamic nuclei (in the territory of the posterior choroidal artery). The syn-
Table 1 Clinical presentation and neuroimaging Case
Clinical presentation
Neuroimaging
Arterial territory involved
.I .nemlcnorea–nemmamsrn . , ., .<.
2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27
CT: no visible lesion CT: r thalamic infarct I hemichorea–hemiballism CT: 1thalamic Iacunar infarct r hemichorea–hemiballism CT: 1parieto occipital and internal capsule hemon’hage r hemichorea–hemiballism CT: leukoaraiosis, 1post capsular infarct r hemichorea–hemiballism CT: left capsulolenticular infarct, Ierrkoencephalopathy r hemichorea–hemiballism CT: I sub-thakunic infarct r hemichorea–hemiballism CT: superficial and deep I MCA infarct r hemichorea–hemiballism CT: r white matter infarct 1hemichorea–hemiballism CT: r old infarct of the head of the caudate, no new lesion r hemichorea–hemiballism CT: 1subacute Ienticular and head of the caudate infarcts r hemichorea–hemiballism CT: 1caudo-putamen and irrtemal capsule infarcts r stereotypic CT: post superficial infarct in the right MCA territory 1stereotypic CT: Ieukoaraiosis, no other visible lesion bilateral jaw myodonia CT: 1subacute frontal parasagittal infarct r hand dystonia and rigidity MRI: I ant / r post fhalamic, pontine, 1cerebella infarcts 1segmental dystonia CT: 1post capsulolenticular infarct r segmental dystonia CT: 1thalamic hemorrhage, 1capsulolenticular infiirct 1hemidystonia CT: 1parieto-tcmporal hemorrhagic infarct r hemidystonia CT: I occipito-temporal, cerebella, 1thalamic infarcts r jerky dystonic unsteady hand MR1: old I pulvinar and lingual gyms infarcts r jerky dystonic unsteady hand CT: r thalamic infarct 1jerky dystonic unsteady hand inaugural 1limb shaking CT: no visible lesion CT: r post borderzone infarct inaugural 1 limb shaking bilateral tremor preceding stroke MRI: bilateral (r > 1)pontine infarct CT: acute r capsulo-thalamic hematoma I astenxis MRI: 1ant paramedian thalamic, r and I cerebella infarcts r astenxis
28 29
r hemiakathisia 1dysartfria and dyskinetic hand
1
MR1: I post thalamic infarct CT: no visible lesion
r PCA: thakrmoperforating, TGA I PCA 1MCA 1PCA: post choroidal 1MCA (LLS) 1PCA 1MCA r McA (LLS) r MCA I MCA (LLS) I McA (LLS) r MCA 1ACA 1PCA I MCA (LLS)) 1PCA+MCA (LLS) 1MCA 1PCA: post choroidal 1PCA: post choroidal r PCA: post cboroidal I MCA (CBF decreased perfusion) r MCA + PCA basilar r PCA 1PCA: tubero-tfralamic, post inf cerebella 1PCA: post choroidal
U: upper extremity; L: lower extremity; F: face; 1:left; r: right; ant: anterior; post: posterior; PCA: posterior cerebral artery; MCA: middle cerebral artery; LLS: lateral lenticulostriate artery; TGA: thalomogeniculate artery; CBF: cerebral blood flow.
‘
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I I
Fig. 1. Summary of the lesions seen in: 1.I and 1.2 hemichorea–hemiballism (1 1 cases); 1.3 and 1.4 hemidystonia (5 cases); 1.5 dyskinesia (2 cases); 1.6 jerky dystonic unsteady hand (3 cases); 1.7 asterixis (2 cases); 1.8 limb-shaking (2 cases).
drome, developed 12 to 18 weeks after the acute stroke in the posterior cerebral artery, which was accompanied by a painful thalamic D6jerine-Roussy syndrome; the delayed hyperkinetic syndromes were characterized by an intense hyperkinetic choreo-atheto-ballic syndrome, together with dystonic posture of the hand and myoclonic-ataxic movements in patients 21 and 22. Patient 20 had right hyperpathia and right hand dystonia with athetosis of the fingers, ataxia and cerebella outflow ‘rubral’ tremor. Limb-shaking (N= 3) in patient 23 was characterized
I
1 Fig. 1 (continued).
1 Fig. 1 (continued),
by a transient brisk arrhythmia shaking of the right arm associated with amaurosis in the left eye in recurring episodes each lasting 2 to 10 rein, which lasted for 3 weeks. Angiography showed left internal carotid occhtsion. On CT, no lesion was visible. On EEG, rare left anterior theta element bursts, were present. SPECT showed a slightly decreased perfusion of the left MCA territory. The hypothesis of repeated transient hemodynamic isI
1
1 . Fig. I (continued).
F. Ghika-Schmid et al./Journal of the Neurological Sciences 146 (1997) 109–116
chemia in the deep left MCA territory was raised. Patient 24 had initial left upper limb-shaking, followed by left facial weakness, visual agnosia and a transient episode of visual hallucination. On CT, a right posterior watershed infarct was found. Thus, initial limb shaking was found in three patients, one with decreased regional cerebral blood flow in the MCA territory, one with posterior watershed infarct, and the third with pontine ischemic lesion. In all three patients this was associated with hemiparesis. The movements were more prominent on the arm than the leg. Two patients had an internal carotid artery stenosis. Patient 25 had intermittent bilateral tremor in the upper extremities preceding a tetraparesis with left hemianesthesia, corticobulbar signs and dysarthria. On MRI, a right paramedian pontic infarct was found in the territory of the paramedian perforating branches of the basilar artery. Focal unilateral asterixis was found in two patients. Patients 26 and 27 had unilateral upper extremity asterixis which occurred in the acute phase of stroke. In the first patient, a sensory-motor hemiparesis was associated and an acute capsular-thalamic hemorrhage was seen on CT, whereas in the second patient hemiparesis only was found on examination and a paramedian thalamic infarct in the territory of the tubero-thalamic artery, together with bilateral hemispheric cerebella infarcts were found on MRI. We found focal action myoclonus of the jaw and tongue in one patient (patient 14) with diffuse leukoaraiosis. The abnormal bilateral myoclonus occurred only when the patient tried to speak, without palatal myoclonus, but with dysarthria, bucco-linguo-facial apraxia, bilateral facial weakness, and hemiparesis involving the right arm. This clinical picture has not previously been reported. The three patients with the jerky unsteady hand syndrome had some degree of action myoclonus. Transient delayed hemiakathisia (N= 1) was found in one patient (patient 28), who presented an acute right hand and foot sensory loss involving all modalities and mild right cortico-spinal signs. On MRI a small infarct was found in the posterior thalamic nuclei involving the pulvinar, probably in the territory of the lateral branches of the left posterior choroidal artery. Five months later he developed kinesiogenic pain on the same side, with features of a D6jerine-Roussy syndrome, which evolved in a few weeks toward a painless urge to move associated with stereotyped movements of the right hemibody (hemiakathisia). The patients with the jerky dystonic unsteady hand syndrome had some feature of restlessness of the hand, which was unable to be kept steady, but no feeling of an urge to move. The summary of the topography of lesions according to the described hyperkinetic syndromes are summarized on Fig. 1. 3.2. Evolution Evolution. All but 4 patients presented acute onset movement disorders concomitant with other deficits. The 4
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patients with delayed syndromes attended the outpatient unit because of the hyperkinesia, but none was expected to occur. The length of the follow-up ranged from 1 week in cases of early regression to 5 years in cases of persistent symptoms. Seven patients were lost from FU. Eleven of 19 untreated patients showed spontaneous regression within 2 weeks. Five patients with hemichorea–hemiballism were treated with haloperidol (doses 1.5 to 9 mg/day) with complete regression within a week, 5 had spontaneous remission without treatment, and one had persistent symptoms. Among the 5 patients with dystonia, only one received clonazepam, with regression within a week, three patients received no treatment, among them two were lost for follow-up and one kept some dystonia of the hand. None of the 3 patients with the jerky dystonic unsteady hand responded to any medication. The hemiakathisia disappeared after a week of clonazepam, and the dysarthria and dyskinetic hand regressed spontaneously without treatment. Six patients showed persistent movement disorder and were unresponsive to all treatment (patients 11, 15, 20, 21, 22 and 23). No patient had recurrent hyperkinetic movement disorders.
4. Discussion Hyperkinetic movement disorders are uncommon in acute stroke, with a prevalence of 29/2500 (1%) and an estimated incidence of 0.08% per year in our hospital-based study. Over the studied period, the total number of patients with subcortical ischemic or hemorrhagic involvement of a large portion of the basal ganglia without causing movement disorders was 536 out of 2500 strokes of any etiology. This observation underlines the rare occurrence of movement disorders in the acute phase of stroke, despite the frequent involvement of the basal ganglia, and could suggest the possibility of strategic locations within the basal ganglia for movement disorders to occur, or peculiar personal idiosyncrasy or features of brain plasticity within these anatomical networks. It is, however, possible that our figures have been underestimated because of the intermittent, transient, spontaneously regressive or delayed nature of their presentation and often the patients or even their family deny that the symptoms were present. The retrospective nature of this study may also lead to an underestimation of prevalence. Indeed in our patients, referred for stroke, the movement disorder was a prominent feature, which resulted in the subsequent examination by a movement disorder specialist, but non obvious presentations of movement disorders may easily escape the attention of non specialists in the field. For these reasons, and because of the large number of patients who were lost for follow up in our outpatient unit after their vascular event, the prevalence of delayed movement disorders cannot be correctly assessed in this study. A lesion involving the basal ganglia (pallidum, puta-
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men, caudate, thalamus) was found in all our cases examined with MRI, whereas the two patients without visible lesion, or the other two ones with lesions involving the hemispherical white matter alone had only CT. These observations suggest that basal ganglia involvement may be critical, although the small number of cases does not allow to rule out the possibility that movement disorders can also occur with superficial lesions not involving the basal ganglia (Ferbert et al., 1990; Shintani et al., 1991; Takeshita et al., 1993). However, this has to be interpreted with caution, because of the small number of MRI scans in our patients. Among basal ganglia, the striatum and pallidum were most frequently involved (44%) (i.e. the territory of the lateral lenticulo-striate arteries), followed by the thalamus (lateral and posterior nuclei) (37Yo)and the subthalamic nucleus (1 case). This observation supports the concept of a global functional network within the basal ganglia (Ghika and Bogousslavsy, 1995; Bhatia and Marsden, 1994) with the interruption of either the direct or the indirect pathway in the basal ganglia by focal lesion. It refutes any clear specificity of the subthalamic nucleus for hemichorea–hemiballism, of the caudate for choreo– athetosis, and of the putamen or globus pallidus for hemidystonia, as already reported (Martin, 1957; Papez et al., 1942; Critchley, 1953; Buruma et al., 1986; Zeman and Whitlock, 1968; Pettigrew and Jankovic, 1985; Burke et al. 1980; L4hercy et al., 1996; Lee and Marsden, 1994; Peterson and Peterson, 1987) and this is in accord with recent studies (D’Olhaberriague et al., 1995; Ghika and Bogousslavsy, 1995; Martin, 1957; LEhercy et al., 1996; Lee and Marsden, 1994; Johnson and Fahn, 1977; Bhatia et al., 1994). As mentioned in these studies, lesions responsible for hemichorea–hemiballism were found in the subthalamic nucleus, but were also found in the thalamus, the pathways interconnecting these nuclei (i.e. in the territory of the perforators of the PCA), the striatum (caudate– putamen) and the pallidum (i.e. in the territory of the deep perforators from the MCA), without involvement of the subthalamic nucleus. ~Similarly, in patients with dystonia, the lesion was located in the territory of the deep perforators from the PCA territory, involving the thalamus, and in two cases the lesion was in the striatum, (i.e. in the territory of the lenticulostriate arteries (LS) from MCA), as previously reported (D’Olhaberriague et al., 1995; Levis and Russo, 1983; Marsden et al., 1985; Ghika and Bogousslavsy, 1995; Martin, 1957; L6hercy et al., 1996; Lee and Marsden, 1994). In the same direction, unilateral asterixis has been reported with infarct in the contralateral fronto– parietal cortex, basal ganglia, cerebellum, thalamus, or brainstem (Young et al., 1976; Degos et al., 1979; Morrey et al., 1979; Shuttleworth and Drake, 1987; Tarsy et al., 1977; Peterson and Peterson, 1987; Bril et al., 1979), which confirms the non-specific nature of asterixis, which can be found with lesions of the sensory-motor system network. The prevalence of unilateral asterixis is probably largely underestimated and has to be looked for and recog-
nized in the acute phase of stroke. Other types of myoclonus found in association with vascular lesions are not specific for any location either. A patient with intention and action myoclonus had a thalamic angioma (Avanzani et al., 1977) and ‘focal reflex myoclonus’ has been reported in a patient with a superficial MCA stroke (Sutton and Mayer, 1974). We found focal action myoclonus of the tongue in only one patient (case 14); this confirms that non epileptic myoclonus seems to be very rare in stroke, and non specific for any topographical location. Tremor was the only movement disorder that we found with a brainstem infarct, but dystonia and asterixis have also been reported in brainstem lesions (Morrey et al., 1979; Baquis et al., 1985; Peterson and Peterson, 1987; Bril et al., 1979). Acute contralateral or ipsilateral stereotypias (Maranganore et al., 1991; Ghika et al., 1995b) had no specificity for any anatomical location. The ‘jerky dystonic unsteady hand syndrome’ (Ghika et al., 1994) is the only hyperkinetic syndrome which was found to be specific for a topographic localization, i.e the posterior thalamic nuclei in the territory of the posterior choroidal artery. Our findings highlight the many subtypes of simple or complex movement disorders (initial, transient, recurrent or delayed) which can be found in stroke involving the basal ganglia, thalamus, sub-cortical white matter and, more rarely, the brainstem. Delayed, recurrent or paroxysmal hemichorea–hemiballism or generalized ballism or chorea (Johnson and Fahn, 1977) or ataxia (Louis et al., 1996) were not seen, but one patient had transient delayed hemiakathisia and three had the delayed ‘the jerky dystonic unsteady hand’ (Ghika et al., 1995a) occurring weeks to months after the acute lesion. All had thalamic infarcts, and this location seems to be one of the best documented strategic anatomical structures for delayed syndromes to occur. Delayed tremor and dystonia have also been reported with lesions in the thalamic nuclei (Kim, 1992). Hyperkinetic movement disorders in stroke occur mostly unilaterally (83Yo),contralaterally to the lesion. We found bilateral asymmetric ballismus, bilateral tremor and limb shaking, and bilateral jaw and tongue myoclonus in 5 patients (17%). Two patients had bilateral lesions (bilateral pontine infarct, leukoaraiosis), but we did not observe abnormal movement strictly ipsilateral to a brain lesion, as reported by others (Peterson and Peterson, 1987; Bril et al., 1979; Moersh and Kemohan, 1939; Dierssen et al., 1961). The limb shaking ipsilateral to the side of the large vessel stenosis may be due to dysfunction in the ipsilateral cerebella pathways. A releasing role played by the ipsilateral lesion allowing an old silent contralateral lesion to be expressed (Bril et al., 1979), or damage to the connections between the sub-thalamic nucleus on each side (Moersh and Kemohan, 1939) can be postulated in such cases. Two thirds of the lesions were small infarcts ( <1.5 mm), often with leukoaraiosis, which incriminates smallvessel disease as the leading cause of stroke, with hypertension (6590) as the most common risk factor. Large-artery
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stenosis was seen with limb shaking, but was otherwise uncommon. As already reported, limb shaking seemed suggestive of hemodynamic problems in the carotid or vertebrobasilar system (Baquis et al., 1985; Fisher, 1962; Hess et al., 1991; Margolin and Marsden, 1982; Yanagihara et al., 1985). Primary hemorrhage was rare. This is in accord with the largest series (D’Olhaberriague et al., 1995). Spontaneous regression of the abnormal movements was seen in half of our patients. Several drugs, including haloperidol, perphenazine, reserpine, tetrabenazine, valproate, chlorpromazine, clonazepam (Adams and Victor, 1993; Dooling and Adams, 1975; Obeso et al., 1984; Milandre et al., 1993; Johnson and Fahn, 1977; Tognetti and Donati, 1986; Bhatia et al., 1994) have been reported to be successful in the treatment of acute hemichorea– hemiballism. Only 3 patients, including 2 with delayed hyperkinetic symptoms resistant to medication, had persistent movement disorders. The nature of this study made it difficult to assess accurately the response to treatment and we will therefore not draw any conclusions from these observations. In conclusion, hyperkinetic movement disorders are infrequent in stroke, but can be found in the acute phase or can be delayed by weeks or months, especially when the lesion in the posterior thalamic nuclei. Generally unilateral, and largely regressive, there may be exceptions to these rules. The clinical pictures are not specific for any anatomical location in a basal ganglia or in the territory of any vessel, except in posterior thalamic nuclei, and this is in accord with the global concept of a complex network with parallel processing in the basal ganglia.
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