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J Neurosurg 121:631–636, 2014 ©AANS, 2014

Emergent surgical embolectomy for middle cerebral artery occlusion due to carotid plaque rupture followed by elective carotid endarterectomy Case report Satoshi Kiyofuji, M.D., Tomohiro Inoue, M.D., Hirotaka Hasegawa, M.D., Akira Tamura, M.D., Ph.D., and Isamu Saito, M.D., Ph.D. Department of Neurosurgery, Fuji Brain Institute and Hospital, Fujinomiya City, Shizuoka, Japan Embolic intracranial large artery occlusion with severe neurological deficit is associated with an extremely poor prognosis. The safest and most effective treatment strategy has not yet been determined when such emboli are associated with unstable proximal carotid plaque. The authors performed emergent surgical embolectomy for left middle cerebral artery (MCA) occlusion, and the patient experienced marked neurological recovery without focal deficit and regained premorbid activity. Postoperative investigation revealed “vulnerable plaque” of the left internal carotid artery without apparent evidence of cardiac embolism, such as would be seen with atrial fibrillation. Specimens from subsequent elective carotid endarterectomy (CEA) showed ruptured vulnerable plaque that was histologically consistent as a source of the intracranial embolic specimen. Surgical embolectomy for MCA occlusion due to carotid plaque rupture followed by CEA could be a safer and more effective alternative to endovascular treatment from the standpoint of obviating the risk of secondary embolism that could otherwise occur as a result of the manipulation of devices through an extremely unstable portion of plaque. Further, this strategy is associated with a high probability of complete recanalization with direct removal of hard and large, though fragile, emboli. (http://thejns.org/doi/abs/10.3171/2014.4.JNS132441)

Key Words • acute ischemic stroke • intracranial embolism • carotid endarterectomy • embolectomy • internal carotid artery stenosis • vascular disorders

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traditional direct surgical embolectomy through a craniotomy for acute ischemic stroke has been performed since the 1950s,9,18 intravenous administration of tissue plasminogen activator and endovascular methods have become recognized as faster and are now the gold-standard treatment for embolism. Most recently, endovascular treatment for acute intracranial large artery occlusion has benefitted from the introduction of new devices, such as the MERCI retriever, lthough

Abbreviations used in this paper: CAS = carotid artery stenting; CEA = carotid endarterectomy; DSA = digital subtraction angiography; DWI = diffusion-weighted imaging; ECG = electrocardiogram; ICA = internal carotid artery; MCA = middle cerebral artery; MRA = MR angiography; NIHSS = National Institutes of Health Stroke Scale; TIMI = Thrombolysis in Myocardial Infarction.

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the Penumbra system, and the Solitaire stent.2,12,13 Recent endovascular embolectomy devices have been used to accomplish up to 80%–90% recanalization rates (Thrombolysis in Myocardial Infarction [TIMI] Grades 2–3), but the complete recanalization rate (TIMI Grade 3) achieved with such devices is not satisfactory, especially when the clot burden is high.2,10,12,17 By contrast, a recent report of surgical embolectomy demonstrated a high complete recanalization rate and an acceptable safety profile, especially when using MRI to select appropriate patients.5 Among cases of devastating acute intracranial large artery occlusion, those arising from intracranial emboli associated with carotid plaque rupture are rare. Given the possible high embolic clot burden associated with ruptured plaque and secondary engrafted thrombus, the treatment strategy for this situation remains controversial. 631

S. Kiyofuji et al. Furthermore, because of proximal, extremely unstable plaque, it can be quite difficult to deploy the endovascular device without generating additional emboli. In the present report we describe a unique case of emergent direct surgical embolectomy through a craniotomy for occlusion caused by ruptured carotid plaque, followed by elective carotid endarterectomy (CEA) to prevent further stroke associated with the extremely unstable plaque.

Case Report History and Examination. A 78-year-old woman with a history of hypertension suddenly collapsed at home and was transported by ambulance to our hospital. She was taking antihypertensive drugs only and had never been treated with any antiplatelet or anticoagulation drugs. Upon arrival, she showed right hemiplegia, global aphasia, and conjugate deviation of her eyes to the left. Her National Institutes of Health Stroke Scale (NIHSS) score was 17. Initial CT showed abnormal high-density signal in the bifurcation of the left middle cerebral artery (MCA), suggestive of some calcified embolus, without any signs of early ischemia (Fig. 1A and B). She was taken to the MRI suite where MR angiography (MRA) demonstrated an occluded M1 on the left, while diffusion-weighted imaging (DWI) showed only minimal ischemia with spotty

high-signal-intensity lesions in the left insular cortex, frontal lobe, and temporal lobe (Fig. 1C–F). Since there was a mismatch between the expected infarction area on MRA and actual lesions on DWI, as well as a mismatch between severe neurological symptoms and minimal lesions on DWI, emergent recanalization treatment was indicated.8,16 Considering the potentially highly calcified appearance of embolic material on CT that could be refractory to the pharmacological effect of intravenous tissue plasminogen activator, in addition to the fact that endovascular service is not available in emergent settings at our institution, we decided, based on our experience with high complete recanalization rates in such procedures, to proceed with emergent surgical embolectomy.5 After a thorough discussion with her family, we started the operation 1.5 hours after the patient’s arrival at our hospital. First Operation. The procedure was conducted as described in detail elsewhere.5 In short, through a left frontotemporal craniotomy, the left MCA bifurcation was exposed. A whitish thrombus was seen from outside the MCA bifurcation (Fig. 2A). A transverse incision was made in the bifurcation, and the apparently partially calcified, hard though fragile embolus was completely removed (Fig. 2B). The incision was sutured with 9-0 nylon (Fig. 2C). Complete recanalization (TIMI Grade 3) was confirmed intraoperatively with an ultrasound Doppler flow meter and immediately postoperatively with an MRA study (Fig. 3). The recanalization time was 42 min-

Fig. 1. Images obtained at patient’s arrival, before the embolectomy. Head CT (A) shows an abnormal high-density lesion (arrow) in the left MCA. The Hounsfield unit count of the emboli (arrow) is 164.9, while those of the sphenoid ridge (bone) and contralateral MCA are 403.2 and 26.4, respectively (B). The left MCA is occluded at M1 (C, arrow), and diffusion-weighted images (D–F) demonstrate high-intensity lesions in the insula, frontal lobe, and temporal lobe.

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Surgical embolectomy followed by carotid endarterectomy

Fig. 2. Intraoperative views of the embolectomy. A white thrombus (A, arrow, near center of image) appeared in the MCA bifurcation and was resected (B). Arteriotomy at the bifurcation was sutured after resection of the thrombus (C).

utes from the start of surgery, 2 hours 32 minutes since the arrival of the patient, and approximately 3 hours 30 minutes since symptom onset.

First Postoperative Course. Postoperatively, the patient showed marked neurological recovery without additional lesions on DWI. She had full restoration of motor function, resulting in an improvement in her NIHSS score from 17 to 5 at 3 weeks postoperatively. Although preoperative and intraoperative electrocardiogram (ECG) did not show atrial fibrillation, a chest radiograph at admission revealed left ventricular hypertrophy. Therefore, we evaluated for possible cardiac embolic causes. Holter ECG and chest ultrasonography by a cardiologist were essentially negative, and thus there was no persuasive evidence of a cardiogenic event. Meanwhile, neck MRI showed only moderate carotid stenosis with a slightly high-intensity lesion in the left carotid plaque on magnetization-prepared rapid acquisition of gradient echo (MPRAGE) imaging, suggesting possible unstable plaque deposition (Fig. 4A–

D).20 We proceeded with digital subtraction angiography (DSA), which demonstrated intermediate stenosis and an irregularly surfaced left internal carotid artery (ICA) with ulceration consistent with ruptured plaque (Fig. 4E). Given these findings, we suspected that the left ICA plaque was the cause of the M1 embolus. At that time, since the patient had regained her premorbid level of activities of daily living, which included ambulating and eating as usual, and after a thorough discussion with her and her family, we decided to proceed with elective carotid endarterectomy (CEA) to remove the embolic origin. Second Operation. The CEA was performed 3 weeks after the surgical embolectomy. Video 1 features actual procedures of the surgical embolectomy and subsequent CEA.

Video 1. Clip demonstrates actual procedures of the surgical embolectomy and subsequent CEA. Copyright Satoshi Kiyofuji. Published with permission. Click here to view with Media Player. Click here to view with Quicktime.

The plaque of the carotid artery is shown in Fig. 5. There were significantly calcified lesions in the plaque, which resembled the embolus in her left MCA bifurcation. Pathological investigation showed similarities between the MCA embolus and the carotid plaque component and revealed that the two specimens were almost identical pathologically. Second Postoperative Course. Postoperative DWI did not show any additional ischemic lesion, and MRA demonstrated a smooth and widely patent left carotid artery. Antiplatelet therapy was started postoperatively instead of anticoagulation therapy, and rehabilitation enabled the patient to live independently. At 6 months postoperatively, her modified Rankin Scale score was 1 without focal neurological deficit.

Discussion

Fig. 3. Magnetic resonance angiogram obtained after the embolectomy. Full recovery of the blood flow of the left MCA was achieved.


Sudden and extremely severe clinical manifestations in patients with ischemic stroke can suggest cardiac embolism associated with atrial fibrillation. About 30% of strokes are associated with atrial fibrillation, and such strokes tend to be devastating.3 Thus, in the featured patient, we initially assumed that the removed embolus was of cardiac origin given the sudden onset of her symptoms, severe neurological deficits, and concomitant cardiomeg633

S. Kiyofuji et al.

Fig. 4. Magnetic resonance angiograms (A–D) of the neck and DS angiogram (E) of the left ICA. Magnetic resonance angiogram of the neck shows the irregular surface of the left ICA (A, arrow), and an MPRAGE image shows high-intensity plaque (B, arrow), which is isointense to low intensity on a T1-weighted image (C, arrow) and isointense to high intensity on a T2-weighted image (D, arrow). Left ICA stenosis was seen on DSA (E, arrow).

aly. Therefore, anticoagulation therapy with heparin followed by warfarinization was started in response to presumed paroxysmal atrial fibrillation. However, a negative postoperative cardiac evaluation directed our attention to the cervical portion of the carotid artery as a possible em-

Fig. 5. Intraoperative view during the CEA. Calcified yellow plaque was present in the internal lumen (arrow), part of which resembled the thrombus that had been resected in the embolectomy (Fig. 2B). An ulcerative lesion was also visible (arrowhead).

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bolic source, despite the fact that cervical MRA showed only low-grade carotid stenosis. Finally, imaging of the plaque using MRI in conjunction with conventional DSA revealed left low-grade carotid stenosis with “vulnerable plaque” as the cause of the embolus. It is quite rare to find that the embolus removed in a surgical embolectomy resembles the ruptured irregular surface and/or contents of the carotid plaque in CEA. Both specimens were hard, yellow, and highly calcified. The pathology report confirmed that the embolus was identical to the ICA plaque in terms of histological features, that is, a highly calcified lesion in the background of some cholesterol crystals. A recent report demonstrated a high rate of recurrent microembolic events, even in low-grade carotid stenosis, once a patient became symptomatic. Indeed, the contents of the plaque were judged as unstable, according to MRI.20 Thus, we need to consider the possibility that even lowgrade carotid stenosis can cause large intracranial emboli, especially when emboli of cardiac origin are excluded. Although there are some case reports on the endovascular removal of distal emboli associated with carotid artery stenting (CAS), direct microsurgical embolectomy of emboli originating from an ICA plaque rupture is quite rare.1,15 Given a potential high clot burden of emboli released from ruptured carotid plaque and the hard but fragile nature of the mixture of calcified plaque with secondary engrafted fibrin clot, it might be difficult to J Neurosurg / Volume 121 / September 2014

Surgical embolectomy followed by carotid endarterectomy achieve appropriate recanalization by pharmacological thrombolysis or endovascular methods. In fact, one study demonstrated that emboli composed of platelet, atheroma, and cellular debris are more resistant than erythrocyterich emboli to any revascularization treatment whether it consists of a fibrinolytic agent, mechanical endovascular embolectomy, or a combination of the two.11 The unusually high Hounsfield unit count and accompanying calcified appearance of the emboli were quite unlikely to be those of simple erythrocyte-rich emboli. By contrast, the high complete recanalization rate and the acceptable safety profile of surgical embolectomy through a craniotomy, regardless of the embolic clot burden, have recently been described.5,14 The safety of the access to an embolic lesion should also be considered. In cases of intracranial major artery embolism coinciding with extremely unstable carotid plaque and possible rupture, endovascular removal of the emboli could involve high risk. If a catheter or guidewire passes through the plaque portion, a thrombus attached to the vulnerable plaque could migrate, causing further distal intracranial embolism. Carotid artery stenting could be tried before removal of the intracranial embolus, but CAS itself is associated with a high risk of distal embolism, especially when the plaque is fragile with ulceration or hemorrhage.4,7 Surgical embolectomy through a craniotomy could be performed to avoid the risk of irritating the vulnerable carotid plaque, while also minimizing the risk of distal emboli during embolectomy, since temporary clips are applied in distal arteries before the removal of emboli.5 Furthermore, in the present case, we preclamped the external carotid artery and common carotid artery to prevent microemboli during the dissection phase of the CEA, which effectively prevented even asymptomatic ischemia, as confirmed on postoperative DWI.6,19 Thus, in cases of intracranial emboli associated with the deposition of unstable carotid plaque, direct surgical embolectomy followed by CEA could have advantages over endovascular treatment from the standpoint of preventing further ischemic events during intervention. The issue of time to reperfusion should be addressed. In theory, surgical embolectomy may take longer than endovascular methods. This is because endovascular methods can be used to achieve recanalization essentially within the same procedure and immediately following diagnostic DSA, whereas surgical embolectomy requires transfer of the patient from the radiology suite to the operating room. To minimize time loss, we made an effort to transport patients directly from the MRI suite to the operating room. Standard frontotemporal craniotomy with minimal hemostasis required about 20 minutes, and in the present case we were able to accomplish recanalization in 42 minutes since the start of surgery and in 2 hours 32 minutes since the patient arrived at our hospital, which, we believe, would compare favorably with the time to recanalization associated with the endovascular method.5 Disclosure The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.


Author contributions to the study and manuscript preparation include the following. Conception and design: Inoue. Acquisition of data: Kiyofuji. Drafting the article: Kiyofuji. Critically revising the article: all authors. Reviewed submitted version of manuscript: all authors. Approved the final version of the manuscript on behalf of all authors: Kiyofuji. Administrative/technical/material support: Hasegawa, Tamura, Saito. References 1. Bielecki D, Goracy J, Lewandowski M, Dabrowski M, Kornacewicz-Jach Z: [Acute thrombosis during carotid artery stenting treated with percutaneous embolectomy in a patient resistant to heparin.] Kardiol Pol 66:559–563, 2008 (Polish) 2. Gobin YP, Starkman S, Duckwiler GR, Grobelny T, Kidwell CS, Jahan R, et al: MERCI 1: a phase 1 study of mechanical embolus removal in cerebral ischemia. Stroke 35:2848–2854, 2004 3. Hannon N, Sheehan O, Kelly L, Marnane M, Merwick A, Moore A, et al: Stroke associated with atrial fibrillation—incidence and early outcomes in the north Dublin population stroke study. Cerebrovasc Dis 29:43–49, 2010 4. Harada K, Morioka J, Higa T, Saito T, Fukuyama K: Significance of combining distal filter protection and a guiding catheter with temporary balloon occlusion for carotid artery stenting: clinical results and evaluation of debris capture. Ann Vasc Surg 26:929–936, 2012 5. Inoue T, Tamura A, Tsutsumi K, Saito I, Saito N: Surgical embolectomy for large vessel occlusion of anterior circulation. Br J Neurosurg 27:783–790, 2013 6. Inoue T, Tsutsumi K, Ohwaki K, Tamura A, Ono H, Saito I, et al: Stratification of intraoperative ischemic impact by somatosensory evoked potential monitoring, diffusion-weighted imaging and magnetic resonance angiography in carotid endarterectomy with routine shunt use. Acta Neurochir (Wien) 155:2085–2096, 2013 7. Iwata T, Mori T, Tajiri H, Miyazaki Y, Nakazaki M: Safety and effectiveness of emergency carotid artery stenting for a high-grade carotid stenosis with intraluminal thrombus under proximal flow control in hyperacute and acute stroke. J Neurointerv Surg 5:40–44, 2013 8. Lansberg MG, Thijs VN, Bammer R, Olivot JM, Marks MP, Wechsler LR, et al: The MRA-DWI mismatch identifies patients with stroke who are likely to benefit from reperfusion. Stroke 39:2491–2496, 2008 9. Meyer FB, Piepgras DG, Sundt TM Jr, Yanagihara T: Emergency embolectomy for acute occlusion of the middle cerebral artery. J Neurosurg 62:639–647, 1985 10. Miteff F, Faulder KC, Goh AC, Steinfort BS, Sue C, Harrington TJ: Mechanical thrombectomy with a self-expanding retrievable intracranial stent (Solitaire AB): experience in 26 patients with acute cerebral artery occlusion. AJNR Am J Neuroradiol 32:1078–1081, 2011 11. Moftakhar P, English JD, Cooke DL, Kim WT, Stout C, Smith WS, et al: Density of thrombus on admission CT predicts revascularization efficacy in large vessel occlusion acute ischemic stroke. Stroke 44:243–245, 2013 12. Penumbra Pivotal Stroke Trial Investigators: The Penumbra Pivotal Stroke Trial: safety and effectiveness of a new generation of mechanical devices for clot removal in intracranial large vessel occlusive disease. Stroke 40:2761–2768, 2009 13. Pereira VM, Gralla J, Davalos A, Bonafé A, Castaño C, Chapot R, et al: Prospective, multicenter, single-arm study of mechanical thrombectomy using Solitaire Flow Restoration in acute ischemic stroke. Stroke 44:2802–2807, 2013 (Erratum in Stroke 44:e239, 2013) 14. Sakai K, Nitta J, Horiuchi T, Ogiwara T, Kobayashi S, Tanaka Y, et al: Emergency revascularization for acute main-trunk occlusion in the anterior circulation. Neurosurg Rev 31:69– 76, 2008

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Manuscript submitted November 3, 2013. Accepted April 30, 2014. Please include this information when citing this paper: published online June 6, 2014; DOI: 10.3171/2014.4.JNS132441. Supplemental online information: Video: http://mfile.akamai.com/21490/wmv/digitalwbc.download. akamai.com/21492/wm.digitalsource-na-regional/jns13-2441_ video.asx (Media Player). http://mfile.akamai.com/21488/mov/digitalwbc.download.akamai. com/21492/qt.digitalsource-global/jns13-2441_video.mov (Quicktime). Address correspondence to: Satoshi Kiyofuji, M.D., Department of Neurosurgery, Fuji Brain Institute and Hospital, 270-12 Sugita, Fujinomiya City, Shizuoka 418-0021, Japan. email: kiyofuji-tky@ umin.ac.jp.
