J Neurosurg 105:142–147, 2006 Hemichorea due to hemodynamic ischemia associated with extracranial carotid artery stenosis Report of two cases RYOMA MORIGAKI, M.D., MASAAKI UNO, M.D., ATSUHIKO SUZUE, M.D., AND SHINJI NAGAHIRO, M.D. Department of Neurosurgery, Faculty of Medicine, The University of Tokushima, Japan U In this paper the authors describe two patients with recurrent hemiparesis and limb shaking that gradually progressed to hemichorea. Cerebral angiography confirmed severe unilateral internal carotid artery stenosis (95%) contralateral to the hemichorea. The cerebral blood flow, assessed using N-isopropyl-p-(iodine-123) iodoamphetamine single-photon emission computed tomography (SPECT), disclosed markedly decreased vascular reserves in both patients. After carotid endarterectomy was performed, the hemichorea gradually subsided and SPECT confirmed increased cerebral perfusion. The results in these cases indicate that surgical revascularization is effective for hemichorea due to cerebral ischemia with reduced vascular reserve. KEY WORDS • carotid endarterectomy • carotid artery stenosis • hemichorea • cerebral blood flow NVOLUNTARY limb shaking is an unusual manifestation of transient ischemic attacks associated with carotid artery occlusive disease; it usually lasts up to 60 seconds.1–3,5–7,9,11–18,20,21,23,26,27,29,30,32–34 In patients with HCHB, another uncommon movement disorder, the involuntary movements are usually continuous and last for weeks or months.4,18,19 Lesions in the contralateral caudate nucleus, putamen, thalamus, subthalamus, pons, midbrain, or subcortical white matter are thought to be responsible for such movement disorders.19 In HCHB, the lesion can be located anywhere in the cortico-striato-pallido-thalamo-cortical feedback loop.8,11 Hemichorea–hemiballism associated with carotid artery occlusive disease is extremely rare: its origin and surgical treatment remain controversial because there is not enough knowledge regarding the cerebral hemodynamic insufficiency in these patients. In this report we evaluate the CBF in two patients suffering from hemichorea and severe extracranial carotid artery stenosis by using 123I-IMP SPECT, and we discuss the efficacy of surgical treatment. This is the first at-rest, acetazolamide-enhanced SPECT study performed before and after CEA to assess the contribution of hemodynamic factors to I Abbreviations used in this paper: CBF = cerebral blood flow; CEA = carotid endarterectomy; ECA = external carotid artery; HCHB = hemichorea–hemiballism; ICA = internal carotid artery; 123 I-IMP = N-isopropyl-p-(iodine-123) iodoamphetamine; MR = magnetic resonance; SPECT = single-photon emission computed tomography. 142 the development of hemichorea associated with severe ICA stenosis. Case Reports Case 1 History. This 75-year-old right-handed man with hypertension, hypercholesterolemia, and a 50-year history of smoking suddenly experienced recurrent transient left hemiparesis. The episodes, which occurred once or twice a week, involved only his left arm and lasted a few seconds. There were no provocative factors. He had no history of convulsive disease, orthostatic hypotension, diabetes mellitus, or parkinsonism. Involuntary continuous trembling of his left arm appeared 1 month after the onset of his first transient ischemic attack; it disappeared during sleep and could be voluntarily suppressed for only a short time. He was admitted to our hospital for further examination. Examination. On admission, the patient was alert. There was very mild upper hemiparesis of his left arm and mild bilateral dysfunction of vibration sensation. There were no carotid artery bruits. In the pronated and supinated positions, the distal portion of his left arm twitched or jerked rapidly; the distal portion of his leg on the same side also shook. His gait was slightly disturbed because of clumsy choreiform left leg movements. The involuntary movements were diagnosed as hemichorea by a neurologist. There was no involuntary movement of the facial muscles. J. Neurosurg. / Volume 105 / July, 2006 Efficacy of CEA in hemichorea due to carotid stenosis Axial T2-weighted MR images revealed small areas of hyperintensity in the bilateral corona radiata (Fig. 1). A right carotid artery angiogram demonstrated severe stenosis (95%) of the right ICA (Fig. 2A) and slow filling of the intracranial arteries (Fig. 2B and C). At-rest 123I-IMP SPECT showed severe hypoperfusion within the right hemisphere (Fig. 3A and D). After acetazolamide was administered, SPECT studies were obtained that revealed a marked decrease in the vascular reserve capacity in the right hemisphere including the basal ganglia (Fig. 3B and E). Operation and Postoperative Course. After a right CEA had been performed, we obtained SPECT studies, which demonstrated improvement in the CBF in the right hemisphere including the basal ganglia (Fig. 3C and F). At 3 months post-CEA, the hemichorea in the patient’s left upper and lower limbs had ceased at rest; it disappeared completely by 2 years. Case 2 History. This 77-year-old woman was admitted to our hospital for evaluation of ICA stenosis demonstrated on MR angiography performed elsewhere. Her history was notable for hypertension, noninsulin-dependent diabetes mellitus, chronic occlusive pulmonary disease, and hypercholesterolemia, but not for convulsive disease, orthostatic hypotension, or parkinsonism. Examination. On admission the patient was alert and without neurological deficits except that her left leg shook intermittently for a few minutes at a time. The involuntary limb movement was transient, brief, and occurred several times a day; during the attacks, the distal portion of her left leg pronated and supinated for approximately 2 or 3 minutes and then the shaking stopped. There were no provocative factors. Over the course of the next 3 months the involuntary left limb shaking progressed to hemichorea when she was awake. Areas of hyperintensity in the head of the caudate nucleus on the right side, bilateral basal ganglia, and centrum semiovale were demonstrated on T2-weighted MR images (Fig. 4). A right carotid artery angiogram showed severe stenosis (95%) of the right ICA (Fig. 5A) and slow filling of the intracranial arteries on the same side (Fig. 5B and C). Atrest SPECT disclosed severe hypoperfusion within the right hemisphere including the basal ganglia (Fig. 6A and D). After acetazolamide was administered, SPECT studies demonstrated a marked decrease in vascular reserve capacity in the right hemisphere including the basal ganglia (Fig. 6B and E). Operation and Postoperative Course. The patient underwent CEA 3 months after the deterioration of her symptoms; subsequently, her hemichorea slowly subsided. Postoperative SPECT demonstrated improved CBF in the right hemisphere including the basal ganglia (Fig. 6C and F). Her hemichorea gradually improved and is apparent only in her gait 18 months after CEA. Discussion We describe two patients whose hemichorea due to a decrease in CBF and vascular reserves in the contralateral hemisphere was associated with ICA stenosis. Because the involuntary movements occurred subsequent to recurrent hemiparesis or intermittent limb shaking, we suspected hemodynamic factors. Our results suggest that hemichorea occurs during the development of hemispheric hypoperfusion and that revascularization may alleviate this symptom. Our search of the literature found only three earlier reports of HCHB associated with major extracranial atheromatous ICA stenosis.8,23,25 In two patients, HCHB showed marked improvement after CEA.23,25 In another patient, the hemichorea gradually subsided naturally; however, there was an incremental worsening of hemiparesis.8 The patient in our Case 1 experienced recurrent transient hemiparesis that progressed to hemichorea, suggesting that increasing involvement of the premotor cortex or corticostriatal fibers resulted in hemichorea. Although an association between moyamoya disease and hemichorea has been reported,10,11, 22,24,28,31 only a few patients described underwent surgical reconstruction.10,11,22,31 After these patients had undergone an ECA–ICA bypass, their hemichorea subsided or disappeared slowly as their CBF normalized. These results suggest that impaired CBF may be an important contributing FIG. 1. Case 1. Axial T2-weighted MR images obtained at admission, showing small areas of high signal intensity in the bilateral corona radiata. L = left; R = right. J. Neurosurg. / Volume 105 / July, 2006 143 R. Morigaki, et al. FIG. 2. Case 1. A: Right carotid artery angiogram showing severe stenosis of the ICA. B and C: Right carotid artery angiograms demonstrating delayed blood flow to the intracranial circulation (A and C, lateral views; B, anteroposterior view). factor in hemichorea associated with intracranial ICA stenosis. It has been reported that HCHB may occur in patients whose areas of ischemia are located within the cortico-stri- ato-pallido-thalamo-cortical feedback loop.8,11 The infarct sites, where CBF is thought to be most severely impaired, and the region of the perfusion defect and decreased reserves must be considered, because the reversible involun- FIG. 3. Case 1. A and D: Preoperative 123I-IMP SPECT scans demonstrating severe hypoperfusion in the right hemisphere including the basal ganglia. B and E: Preoperative 123I-IMP SPECT scans obtained after acetazolamide infusion, showing a marked decrease in the vascular reserve in the right hemisphere including the basal ganglia. C and F: Postoperative 123I-IMP SPECT scans demonstrating improvement in the CBF in the right hemisphere including the basal ganglia. 144 J. Neurosurg. / Volume 105 / July, 2006 Efficacy of CEA in hemichorea due to carotid stenosis FIG. 4. Case 2. Axial T2-weighted MR images obtained at admission, showing small areas of high signal intensity in the right white matter in the frontal lobe and bilateral basal ganglia. tary movements differed in earlier reports in patients with HCHB associated with carotid occlusive disease. Many infarcts occur in the frontal subcortical white matter8,10,11,25,27 and basal ganglia infarcts are relatively rare.10,23,25 Although in earlier reports the area of decreased CBF varied from the cortex to the basal ganglia,8,10,11,25 the region of decreased vascular reserves involved the frontal lobe in two of three cases.10,11 This suggests that lesions on the anterior border zone are associated with the greatest consequence. The infarcts in our patients were located in the deep anterior watershed (Case 1) and the frontal centrum semiovale and basal ganglia (Case 2), regions considered to lie within the anterior watershed area. The regions of decreased perfusion and autoregulatory reserve were hemispheric. Our results support the hypothesis that connecting fibers in the superficial or deep anterior watershed were exposed to ischemic conditions and that the selective disruption of corticostriatal projections from the indirect pathway resulted in the hemichorea observed in our patients. Conservative medical therapies have been attempted in patients with limb shaking. Administration of antiplatelet agents and lowering the dose or discontinuing administration of antihypertension agents have resulted in marked improvement in some cases.1,2,16,23,30 Anticonvulsion agents and levodopa have been ineffective in most patients.1,2,12,32,34 The most common and effective treatments are surgical revascularization, for example, CEA,1,2,14,20,29,32,33 CEA specific to the ECA,14,33,34 and ECA–ICA bypass surgery.1,5,7,9,11,13,32,33 In FIG. 5. Case 2. A: Right carotid aftery angiogram demonstrating severe carotid artery stenosis. B and C: Right carotid artery angiograms showing stenosis of the ICA at the supraclinoid portion and slow filling of the intracranial middle cerebral artery (A and C, lateral views; B, anteroposterior view). J. Neurosurg. / Volume 105 / July, 2006 145 R. Morigaki, et al. FIG. 6. Case 2. A and D: Preoperative 123I-IMP SPECT scans showing severe hypoperfusion in the right hemisphere including the basal ganglia. B and E: Preoperative 123I-IMP SPECT scans obtained after acetazolamide infusion, revealing a marked decrease in vascular reserve in the right hemisphere including the basal ganglia. C and F: Postoperative 123IIMP SPECT scans demonstrating improved CBF in the right hemisphere including the basal ganglia. some patients with spontaneous collateral compensation, a natural cure is obtained, whereas in others the condition may progress to hemichorea. Although in many patients infarct lesions appeared in the frontal white matter,1,2,7,11,30,33,34 in others there were no lesions.1,2,14,29,32,33 The region involved in the perfusion defect frequently includes the frontoparietal lobes,6,7,11,12,29,30,34 and decreased vascular reserves are often hemispheric.2,5,7,12,14 There is some evidence for a correlation between limb shaking and ischemia in the anterior border zone. We suggest that decreased vascular reserves constitute a risk factor for the progression of limb shaking to HCHB. In addition we stress that before undertaking any revascularization procedures, the status of a patient’s cerebrovascular reserves must be determined. We propose that the mechanism underlying the development of hemichorea associated with carotid artery occlusive disease is strongly correlated with ischemia in the anterior border zone and that surgical revascularization is an effective therapy in these patients. Cytotoxic edema appears to be an unlikely candidate for the cause of treatable involuntary movements in our Case 2 because the patient’s leg shaking continued for 3 months and gradually worsened in the absence of further infarctions. Conclusions We describe two patients with severe hemodynamic ischemia due to severe carotid artery stenosis who manifested 146 hemichorea. Carotid endarterectomy effectively improved this rare disorder and normalized the CBF. References 1. Baquis GD, Pessin MS, Scott RM: Limb shaking—a carotid TIA. Stroke 16:444–448, 1985 2. Baumgartner RW, Baumgartner I: Vasomotor reactivity is exhausted in transient ischaemic attacks with limb shaking. J Neurol Neurosurg Psychiatry 65:561–564, 1998 3. Bogousslavsky J, Regli F: Unilateral watershed cerebral infarcts. Neurology 36:373–377, 1986 4. Dewey RB Jr, Jankovic J: Hemiballism-hemichorea. Clinical and pharmacologic findings in 21 patients. Arch Neurol 46:862–867, 1989 5. 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