Clinical Neurology and Neurosurgery 111 (2009) 695–698
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Case report
Treatment of limb-shaking TIAs with external carotid artery stenting L. Christine Turtzo a,∗ , Philippe Gailloud b , Rebecca F. Gottesman c a
Department of Neurology, University of Connecticut Health Center, MC 1840, 263 Farmington Avenue, Farmington, CT 06030, United States Division of Interventional Neuroradiology, Johns Hopkins School of Medicine, Baltimore, MD, United States c Division of Cerebrovascular Neurology, Johns Hopkins School of Medicine, Baltimore, MD, United States b
a r t i c l e
i n f o
Article history: Received 18 September 2008 Received in revised form 24 April 2009 Accepted 26 May 2009 Available online 25 June 2009
a b s t r a c t Limb-shaking transient ischemic attacks (TIAs) occur when perfusion is reduced to the cortical territory associated with the transient movements. We present a case in which a patient with preexisting left internal carotid artery (ICA) occlusion developed limb-shaking TIAs secondary to severe stenosis of her left external carotid artery (ECA). After angioplasty and stenting of her left ECA, her symptoms resolved. © 2009 Elsevier B.V. All rights reserved.
Keywords: Limb-shaking TIA External carotid artery Carotid artery occlusion Stenting Angioplasty Transient ischemic attack
1. Introduction Classical TIAs are transient neurological deficits that may include difficulties with language, weakness, numbness, or visual loss, and are considered to be warning signs of impending stroke. A much less common form is the limb-shaking TIA, in which the patient experiences transient rhythmic movements, typically under conditions that would lead to reduced cerebral perfusion [1,2]. These involuntary movements may be initially mistaken for focal motor seizures [3–5], and are highly associated with severe extracranial or intracranial ICA occlusive disease [6] or stenoses of the anterior or middle cerebral arteries [7]. In this case report we present a patient with a longstanding left ICA occlusion, in whom the development of limb-shaking TIAs was the manifestation of a severe left ECA stenosis. 2. Case report A 77-year-old female presented with transient episodes of right hand clumsiness and right arm-shaking. She had first noticed that she would periodically drop objects from her right hand and experience trembling of her right forearm and hand. At times, these episodes would be accompanied by right leg weakness and/or slurred speech. The events occurred with changes in position, and her symptoms resolved within seconds of her lying down. After an
∗ Corresponding author. Tel.: +1 860 679 8939; fax: +1 860 679 1181. E-mail address:
[email protected] (L.C. Turtzo). 0303-8467/$ – see front matter © 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.clineuro.2009.05.010
episode, she would feel tired and thirsty for an hour. The events occurred at most once a day, and had been stable in duration for over a month. Her past medical history was notable for a coronary artery bypass, hypertension, macular degeneration, and left subclavian artery occlusion. She also had a history of clipped right posterior communicating artery aneurysm, left ICA endarterectomy with subsequent restenosis, followed by stenting and eventual occlusion, and severe left vertebral artery stenosis. Despite her extensive history of cerebrovascular disease, at the time of presentation, she had no evidence of major stroke either clinically or radiologically. She also had an extensive history of tobacco smoking, which she had ceased 10 years previously. Several months prior to presentation, she had been taking high dose atorvastatin, but this was stopped secondary to elevated liver function tests (LFTs). She had been managed with warfarin and aspirin for management of a symptomatic left vertebral artery stenosis. Two months prior to the development of the limb-shaking events, she developed an acute gastrointestinal bleed, and she was transitioned from warfarin and aspirin to clopidogrel. She was also being managed with permissive hypertension. Her blood pressure at presentation was 140/80 in the right arm (her blood pressure was unobtainable in her left arm secondary to her subclavian artery stenosis), with no evidence of orthostasis. Her neurological examination was notable for mild short-term memory problems, a slight ptosis of her right eyelid, and flattening of her left nasolabial fold, although voluntary facial movements were symmetrical. Her motor, sensory, reflex, gait and coordination examinations were normal.
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Fig. 1. MRI imaging at presentation. Note the presence of small vessel ischemic changes on (A) FLAIR imaging, but the absence of acute changes on (B) diffusion-weighted imaging (DWI).
She underwent an MRI (Fig. 1), which showed no evidence of acute stroke. An EEG demonstrated no evidence of epileptiform activity. She was further titrated from her antihypertensive medication to allow permissive hypertension, and her atorvastatin was restarted at a lower dose since her LFTs had normalized. CT angiography was obtained but was difficult to interpret due to the presence of heavily calcified vessels. She underwent a four-vessel cerebral angiogram for additional clarification of her cerebrovascular status, which documented a high-grade stenosis of her left ECA (Fig. 2A). Her left ECA stenosis was thought to be a significant contributor to her limb-shaking TIA symptoms because of the degree of collateral flow she received to her left hemisphere via that vessel (Fig. 3). While an outpatient procedure was being planned, she began having recurrent episodes of right-sided weakness and armshaking, despite management with clopidogrel, aspirin, and atorvastatin. She was admitted to the hospital, where an MRI showed no evidence of acute infarction. An urgent angiogram showed that her left ECA stenosis had worsened. Stent place-
ment with pre- and post-deployment balloon angioplasty was performed, with excellent restoration of flow (Fig. 2B). The patient tolerated the procedure well, with no neurological deficits postoperatively. She was maintained on clopidogrel and aspirin after stenting, and did well from a neurological perspective with no recurrences of her limb-shaking TIAs. Approximately 6 months after her ECA stenting, she developed unstable angina and underwent coronary artery stenting, with continuation of both clopidogrel and aspirin afterwards for maintenance of her coronary stent. Approximately 10 months after this procedure, she began experiencing episodes of right hand weakness, ultimately leading to postural episodes of right-sided limb-shaking. This was despite maximal medical therapy and permissive hypertension. She was hospitalized once again, and again had no acute infarction by MRI, although MR perfusion imaging documented low perfusion to her left cerebral hemisphere (Fig. 4). An urgent angiogram showed some restenosis of the left ECA but also a new critical stenosis at the
Fig. 2. Digital subtraction angiography, left common carotid artery, nonsubtracted lateral view (A) at presentation. Note the occluded left ICA stent (thick arrow) and the significant stenosis of the left ECA (thin arrow). (B) Left common carotid artery, nonsubtracted lateral view post-angioplasty and stenting of left ECA.
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Fig. 3. Digital subtraction angiography. (A) Right common carotid injection, anteroposterior view; (B) left common carotid injection, anteroposterior view; (C) right common carotid injection, lateral view; (D) left common carotid injection lateral view. Note the absence of flow from the occluded left ICA, and the collateral flow from the left ECA.
origin of the left vertebral artery, in the setting of her occluded left subclavian artery. She underwent urgent angioplasty and stenting of the left vertebral artery origin stenosis, with successful resolution of flow to the left hemisphere through a patent posterior communicating artery. Her symptoms resolved and she did not have return of symptoms nor any new TIA’s for at least 1.5 years following this intervention.
3. Discussion
Fig. 4. MR time to peak perfusion (TPP) image obtained upon recurrence of patient’s limb-shaking TIA symptoms 10 months after angioplasty and stenting of left ECA. Note the decreased perfusion in the left cerebral hemisphere.
This case illustrates a patient with a prior left ICA occlusion, in whom development of a left ECA stenosis precipitated limb-shaking TIAs. She was successfully treated by angioplasty and stenting of her left ECA. In patients with ICA occlusion, the ECA can become an important source of collateral flow to the brain [8,9], as in our patient. When she developed stenosis in her ECA, she manifested, under conditions precipitating cerebral hypoperfusion, rhythmic limb-shaking movements. After stenting and angioplasty of her original ECA stenosis, her symptoms resolved. Ten months later, however, she had developed limb-shaking TIAs once again. While she had some degree of restenosis of her ECA, her left vertebral artery stenosis had progressed to a critical degree. This, in conjunction with her left subclavian artery occlusion and carotid disease, resulted in subclavian steal syndrome during high demand states, resulting in reemergence of her limb-shaking TIAs due to difficulties perfusing her left cerebral hemisphere.
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Prior to her presentation, our patient’s cerebrovascular disease had been medically managed, but was complicated by medication side effects which led to changes from the ideal protocol. For prevention of stroke, per American Heart Association/American Stroke Association guidelines [10], her medical team had her on an antiplatelet, a statin, and antihypertensives, and the patient had ceased smoking several years previously. She was also on warfarin, which had been started in an attempt to manage her vertebral artery stenosis. Her blood glucose has always been normal, requiring no antidiabetic management to date. At the time she presented to us with limb-shaking TIAs, her statin had been held secondary to elevated LFTs, and she had been taken off aspirin and warfarin due to recent gastrointestinal bleeding. In light of the Warfarin–Aspirin Symptomatic Intracranial Disease (WASID) trial results, which showed no benefit of warfarin over aspirin in the management of intracranial disease and an increased risk of bleeding with warfarin [11], our patient’s lack of benefit from the combination of warfarin and aspirin and development of gastrointestinal bleeding is not surprising. Her statin was restarted at a lower dose once her LFTs improved, and titrated up as tolerated to achieve better cholesterol control. Once she developed further stenosis of her cerebral vessels, causing further difficulties with left hemisphere perfusion, strict blood pressure control could no longer be maintained, as this exacerbated her limb-shaking TIA episodes. After her interventions, our patient’s antihypertensive therapy has been reinstated at low doses, with her now tolerating systolic blood pressures of 140–160 mm Hg without return of her symptoms. Treatment of limb-shaking TIAs has been reported in a series of case reports, but no controlled clinical trials. Patients who are poor surgical candidates have been managed medically, with antiplatelet agents, antilipid agents, and modification of antihypertensive control [2,5,6]. Successful internal carotid endarterectomy [6,12] and external carotid endarterectomy [13] have been documented in case reports for the treatment of limb-shaking TIAs. A randomized clinical trial using flow monitoring techniques to select appropriate patients with ICA occlusion for external carotid–internal carotid (EC–IC) bypass is currently underway (the Carotid Occlusion Surgery Study [COSS]; http://www.cosstrial.org/coss/home.asp), but whether EC–IC bypass will be validated for patients with ICA occlusion and limb-shaking TIAs is currently unknown. In patients who are at high surgical risks, angioplasty and stenting is an option for treatment of symptomatic ICA stenosis [14] or symptomatic ECA stenosis [15,16], although no such procedures have been reported to date in patients with limb-shaking
TIA. Potential risks of endovascular revascularization include vasospasm during device deployment, dissection, embolization, acute stent thrombosis, stroke, and post-procedural hypotension and/or bradycardia [17]. The case described here is the first documentation of any form of limb-shaking TIA successfully treated with carotid artery angioplasty and stenting. References [1] Tatemichi TK, Young WL, Prohovnik I, Gitelman DR, Correll JW, Mohr JP. Perfusion insufficiency in limb-shaking transient ischemic attacks. Stroke 1990;21:341–7. [2] Ali S, Khan MA, Khealani B. Limb-shaking transient ischemic attacks: case report and review of literature. BMC Neurol 2006;6:5. [3] Niehaus L, Neuhauser H, Meyer BU. Hemodynamically-induced transitory ischemic attacks. A differential focal motor seizures diagnosis? Nervenarzt 1998;69:901–4. [4] Niehaus L, Neuhauser H, Meyer BU. Transient visual blurring, retro-orbital pain and repetitive involuntary movements in unilateral carotid artery occlusion. Clin Neurol Neurosurg 1998;100:31–2. [5] Schulz UG, Rothwell PM. Transient ischaemic attacks mimicking focal motor seizures. Postgrad Med J 2002;78:246–7. [6] Baquis GD, Pessin MS, Scott RM. Limb shaking—a carotid TIA. Stroke 1985;16:444–8. [7] Han SW, Kim SH, Kim JK, Park CH, Yun MJ, Heo JH. Hemodynamic changes in limb shaking TIA associated with anterior cerebral artery stenosis. Neurology 2004;63:1519–21. [8] Jackson BB. The external carotid as a brain collateral. Am J Surg 1967;113:375–8. [9] Zarins CK. Revascularization of the external carotid artery. J Vasc Surg 1985;2:232–4. [10] Adams RJ, Albers G, Alberts MJ, et al. Update to the AHA/ASA recommendations for the prevention of stroke in patients with stroke and transient ischemic attack. Stroke 2008;39:1647–52. [11] Chimowitz MI, Lynn MJ, Howlett-Smith H, et al. Comparison of warfarin and aspirin for symptomatic intracranial arterial stenosis. N Engl J Med 2005;352:1305–16. [12] Salah Uddin ABM. Limb shaking transient ischemic attack—an unusual presentation of carotid occlusive disease. A case report and review of the literature. Parkinsonism Relat Disord 2004;10:451–3. [13] Klempen NL, Janardhan V, Schwartz RB, Stieg PE. Shaking limb transient ischemic attacks: unusual presentation of carotid artery occlusive disease: report of two cases. Neurosurgery 2002;51:483–7 (discussion 487). [14] Shawl F, Kadro W, Domanski MJ, et al. Safety and efficacy of elective carotid artery stenting in high-risk patients. J Am Coll Cardiol 2000;35:1721–8. [15] Eisenberg JA, Dimuzio PJ, Carabasi A, Larson R, Lombardi JV. Endovascular repair of symptomatic external carotid artery stenosis. J Vasc Surg 2005;42: 1210–2. [16] Adel JG, Bendok BR, Hage ZA, Naidech AM, Miller JW, Batjer HH. External carotid artery angioplasty and stenting to augment cerebral perfusion in the setting of subacute symptomatic ipsilateral internal carotid artery occlusion. Case report. J Neurosurg 2007;107:1217–22. [17] Liapis CD, Bell PR, Mikhailidis D, et al. ESVS guidelines. Invasive treatment for carotid stenosis: indications, techniques. Eur J Vasc Endovasc Surg 2009;37:1–19.