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Occurrence and Prognostic Significance of Cervical Pseudodissection Phenomenon Associated with Acute Intracranial Internal Carotid Artery Occlusion Category
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OF-CERVICAL-PSEUDODISSECTION-PHENOMENON) Clinical Investigative Study Occurrence and Prognostic Significance of Cervical Pseudodissection Phenomenon Associated with Acute Intracranial Internal Carotid Artery Occlusion Farhan Siddiq, MD, Saqib A. Chaudhry, MD, Paramita Das, MD, Rakesh Khatri, MD, Gustavo Rodriguez, MD, Adnan I. Qureshi, MD From the Zeenat Qureshi Stroke Research Center, University of Minnesota - Neurology, Minneapolis, MN. Keywords: Acute stroke, carotid artery dissection, pseudodissection, revascular- ization. Acceptance: Received February 17, 2012, and in revised form May 14, 2012. Accepted for publication June 22, 2012. Correspondence: Address correspon- dence to Adnan I. Qureshi, MD, Ex- ecutive Director, Minnesota Stroke Ini- tiative, Associate Head, Department of Neurology, Professor of Neurology, Neu- rosurgery, and Radiology, University of Minnesota, 12-100 PWB, 516 Delaware St. SE, Minneapolis, MN 55455. E-mail:
[email protected]. J Neuroimaging 2013;23:384-390. DOI: 10.1111/j.1552-6569.2012.00741.x A B S T R A C T BACKGROUND Acute stroke from intracranial internal carotid artery (ICA) occlusion can occasionally resemble angiographic cervical ICA dissection which may cause delays in endovascular acute ischemic stroke treatment. OBJECTIVE To determine the angiographic characteristics of the phenomenon of “pseudodissection” and its clinical implications in acute ischemic stroke endovascular treatment. MATERIAL AND METHODS Retrospective analysis of angiographic and clinical data from 31 patients with ischemic acute stroke secondary to intracranial ICA occlusion, treated with endovascular therapy at two University-affiliated institutions, was performed. Pseudodissection was defined as angiographic appearance of typical cervical ICA dissection with evidence of normal inner vascular wall upon further catheter exploration. RESULTS Angiographic appearance pseudodissection was identified in 7 out of 31 patients (22.6%). Six patients had guide catheters placed proximal to pseudodissection in anticipation of stent placement for treatment of ICA dissection. All 7 patients had further exploration of the presumed dissected segment (6 microcatheter, 1 diagnostic catheter) which demon- strated normal vascular inner wall. The clot was located more commonly in the petro- cavernous segment in the pseudodissection patients (5/7, 71%). Carotid terminus clot was more common in ICA occlusion patients than pseudodissection patients (18/24, 75% vs. 2/7, 29% respectively, P < .0001). Recanalization was less common in pseudodis- section patients compared to ICA occlusion patients (3/7 and 21/24 respectively, P = .029). CONCLUSION Early recognition of pseudodissection in the ICA is important in the setting of acute ischemic stroke to avoid delay in treatment of intracranial ICA occlusion. Introduction Over the past decade, several advances have been made in the endovascular treatment of acute ischemic stroke. Subse- quent to the results of Interventional Management of Stroke (IMS) and Intra-arterial Prourokinase for Acute Ischemic Stroke (PROACT II) trial,1,2 increasing number of ischemic stroke patients are expected to be treated with pharmacological and/or mechanical endovascular treatment. Emergent cerebral angiog- raphy performed as a prerequisite to endovascular treatment has revealed unique findings such as development of collat- erals and arteriovenous shunting.3−5 In anecdotal procedures, we have noticed that emergent angiogram demonstrates find- ings consistent with internal carotid artery (ICA) dissection, which spontaneously resolve after recanalizing tandem occlu- sions. Since emergent stent placement would be frequently considered as treatment for recanalization of ICA in such sce- narios,6,7 we choose to further characterize the finding of “pseu- dodissection” to avoid unnecessary procedures and delay in ad- dressing primary intracranial tandem lesions. In this report, we describe the clinical and angiographic features of patients who presented with an initial angiographic appearance of pseudodis- section in cervical ICA among a consecutive series of patients with acute intracranial ICA occlusion. Material and Methods Data Collection All patients who were treated with endovascular therapy for acute ischemic stroke at two University-affiliated comprehen- sive stroke centers from January 2008 to March 2011 were 384 Copyright C 2012 by the American Society of Neuroimaging
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Fig 1. Reference sample of a classic cervical ICA dissection result- ing in a flame-shaped occlusion.11 identified from a prospectively collected data in a standardized format. All patients with acute ICA occlusion were reviewed. Angiographic images of all these patients were reviewed by en- dovascular surgical neuroradiology fellows (Siddiq, Khatri) and patients who had findings consistent with ICA dissection were further reviewed by an endovascular surgical neuroradiology faculty (Rodriguez, Qureshi). Definition of Angiographic ICA Dissection The classical angiographic appearance of ICA dissection has been described as irregular lumen (string sign, flame-shaped oc- clusion), double lumen, and intimal flaps.8−10 For the purpose of this study, flame-shaped occlusion with or without string sign on angiography was considered as inclusion criteria. Reference sample angiogram of a classic ICA dissection is provided in Figure 1.11 “Pseudodissection” was defined as appearance of classical “flame-shaped occlusion” with or without “sting sign” in the cervical ICA at the time of initial diagnostic angiography for acute ischemic stroke treatment and three of the following four features: 1. Occlusion of the ICA by a clot distal to the pseudodissection site, evident upon endovascular exploration of the dissected segment. 2. No evidence of vessel wall damage, double lumen or intimal flap at the site of pseudodissection on angiographic images obtained from multiple microcatheter injections within the arterial segment with flame-shaped occlusion. 3. Resolution of abnormality without any specific treatment after recanalization of distal occlusion. 4. No evidence of atherosclerotic lesion at the site of pseudodissec- tion. After the final screening, clinical and further radiographic data were collected for the selected patients from the hospital charts. This included patient’s age, gender, findings of com- puted tomographic (CT) angiogram prior to the procedure, site of occlusion, endovascular approach utilized, results of the en- dovascular treatment, National Institutes of Health stroke scale (NIHSS) score at presentation, at the time of discharge, and modified Rankin scale at 3 month follow-up. The pre- and postprocedure severity of occlusion was ascertained by one investigator for all 31 patients after review of pertinent angio- graphic images. Angiographic recanalization was defined by ei- ther partial or complete recanalization upon completion of the procedure. Results Illustrative Case A 74-year old woman with past medical history significant for hypertension and atrial fibrillation, on warfarin [International Normalized Ratio (INR) value of 2.4], was found to have left hemiplegia with right gaze preference on the morning of pre- sentation. Her NIHSS score at presentation was 18. She under- went a computed tomography (CT) angiogram with perfusion study demonstrating complete occlusion of the right cervical ICA, increased mean transit time with decreased flow, and pre- served volume in the right middle cerebral artery territory. She was considered outside the window period for intravenous thrombolysis due to unknown time of onset; however, based on CT perfusion results suggesting potentially salvageable tissue in the right middle cerebral artery territory, a decision was made to emergently take her to angiographic suite for endovascular revascularization. After the femoral sheath placement, a Simmons II diag- nostic catheter was advanced into the right common carotid artery. Diagnostic angiogram demonstrated slow flow in the right ICA with findings consistent with arterial dissection be- yond the carotid bulb. The lateral projection demonstrated “flame-shaped occlusion” (Fig 2a, Serial no. 6). Simmons II catheter was then exchanged with a 6 French MPD Envoy guide catheter (Cordis R© Corp., Miami Lakes, FL, USA) over a stiff exchange glide wire in anticipation for a possible stent placement. Prowler Plus microcatheter (Codman R© Johnson & Johnson Med. Ltd., Wokingham, UK) was advanced into the right ICA over a TransendTM Ex microwire (Boston Sci., Ntick, MA, USA). Once it was determined that the actual site of oc- clusion was at petro-cavernous segment of right ICA, the MPD guide catheter was advanced into the origin of right ICA. An angiogram at this site demonstrated normal cervical segment of right ICA (Fig 2b, Serial no. 6). The intra-arterial thrombolysis was attempted with intra-arterial infusion of integrilin in right ICA and right anterior cerebral artery (A1 segment), and right middle cerebral artery (M1 segment) angioplasty. There was no Siddiq et al: Prognostic Significance of Pseudodissection Phenomenon 385 Fig 2. Angiographic data: Column 1: serial numbers. Column 2: (A) Initial diagnostic angiogram of ICA showing findings consistent with dissection or pseudodissection. Column 3: (B) Evidence of intact inner arterial wall or involved ICA showing no evidence of proximal dissection. improvement of flow in the right middle cerebral artery after angioplasty and integrilin infusion. Procedure was discontinued at that point. Patient Characteristics After the initial screening, 31 patients were identified who had endovascular treatment of acute stroke due to ICA occlusion. Out of these 31, a total of 7 patients (22.6%) fulfilled the crite- ria for “pseudodissection.” The clinical characteristics of these 7 patients are provided in Table 1. The angiographic data demon- strating the evidence of pseudodissection are shown in Figure 2. Since our study was limited to patients with intracranial ICA oc- clusion, none of the other patients in our study met the criteria for true dissection after detailed evaluation of the angiogram. Mean age of these 7 patients was 62 years (range 17-82 years). There were 4 women and 3 men. The median NIHSS score at the time of presentation was 15 (range 9-22). The initial CT angiogram was suggestive of carotid artery occlu- sion at its origin in all 7 patients. Upon initial diagnostic an- giography, suspicion of cervical ICA dissection was raised in all 7 patients based on flame-shaped occlusion/near occlu- sion (Fig 2). Diagnostic catheters were then exchanged with either a 6 French Cook R© Shuttle (Cook Inc., Bloomington, IN, USA) (patients 1, 3, and 7) or a 6 French MPD En- voy guide catheter (Cordis R© Corp., Miami Lakes, FL, USA) (patients 4, 5, and 6). Guide catheters were advanced till the distal common carotid artery in anticipation for a stent placement in the cervical segment of ICA. Microcatheter 386 Journal of Neuroimaging Vol 23 No 3 July 2013 Table 1. Basic Demographics for Patients with Pseudodissection Serial # Age Sex Seg. of ICA Occluded Endovasc. Treatment Recanalization Adm. NIHSS Score Dis. NIHSS Score 3m mRS 1 17 F Right petro-cavernous Alteplase, angioplasty Yes 9 0 0 2 82 F Right carotid terminus Alteplase No 13 11 No follow-up 3 45 M Left petro-cavernous TNK No 14 5 1 4 59 M Left petro-cavernous Altiplase, Angioplasty Yes 22 14 No follow-up 5 82 F Left petro-cavernous TNK,
Alteplase Angioplasty Yes 11 Death Death 6 74 F Right carotid terminus Integrilin, Angioplasty No 18 12 4 7 76 M Left petro-cavernous Alteplase, Merci No 21 Death Death Legends: Seg: Segment; TNK 3m mRS: 3 month modified Rankin scale, NIHSS: National institutes of Health Stroke scale; Adm: Admission; Dis: Discharge. Table 2. Comparison between Patients with ICA Occlusion with or without Angiographic Pseudodissection Pseudodissection Absent Present Total 24 7 P value Age 65.9 ± 16.1 62.4 ± 23.6 .725 Female 13 (54%) 4 (57.1%) .889 Admission NIHSS score 15.9 ± 6.9 15.4 ± 4.9 .53 Location of thrombus Petro-cavernous segment 0 5 (71%) ters the tunica media and tracks cranially to form an intra- mural hematoma.18−20 The mass effect from the hematoma and/or intimal disruption may cause parent vessel narrow- ing or occlusion, which is evident as “flame-shaped” occlu- sion on conventional angiography. A typical contrast-enhanced CT angiogram depicts a narrow eccentric lumen surrounded by crescent-shaped mural thickening and peripheral enhance- ment,21 which are considered specific signs but are not very sen- sitive.22,23 The most common findings on a digital subtraction angiogram are: “string sign,” “tapering stenosis,” and “flame sign.”9 Other pathognomonic features of dissection such as inti- mal flap or double lumen are found in less than 10% of cases.9,24 The “flame” sign is a tapered occlusion that usually spares the carotid bulb. This sign is considered to be highly suggestive of a dissection when visualized in the ICA25 particularly in the settings of acute ischemic stroke. It is important to recognize ICA dissection in an acute stroke patient because it carries important implications. The treatment and outcomes differ for ischemic strokes related to carotid dis- section compared with strokes related to embolic phenomenon or thrombosis of an atherosclerotic lesion. Intravenous and intra-arterial thrombolysis procedures have lower rates of fa- vorable outcome among patients with ischemic stroke related to ICA dissection.26 Presence of arterial dissection is associated with poor outcome and higher mortality.26,27,28 The treatment for acute thromboembolism includes intra- arterial thrombolysis delivered by microcatheter directly into the clot,2 mechanical retrieval of clot by Mechanical Embolus Removal in Cerebral Ischemia (MERCI) devices (Concentric Medical, Mountain View, CA, USA),29,30 disruption and aspira- tion of clot with Penumbra Stroke System (Penumbra, Alameda, CA),31,32 and/or intracranial angioplasty with or without and stent placement.33,34 Due to prominent differences in outcome among patients with acute ischemic stroke related to dissec- tion, a different approach emphasizing on endovascular stent placement has been proposed.7,35,36 Even though intra-arterial thrombolysis may be a safe method for treatment of acute stroke from cervical ICA dissection,37 Lavalle et al38 found that clin- ical outcomes may be better in patients treated with stent and thrombolysis as compared to those treated with intravenous thrombolysis alone. The current paradigm focuses on cervical ICA recanaliza- tion using stent placement followed by treatment of the tandem lesion using thrombolytics and mechanical maneuvers.39 Other variations in technique include avoiding occlusive balloon in- flation in the ICA as part of flow arrest (while using MERCI devices), and avoiding mechanical disruption in the proxim- ity of the dissection to prevent any worsening of dissection. Intravenous or intra-arterial GPIIa/IIIb inhibitors may be ad- ministered in anticipation of emergent stent placement. Such steps delay the approach to primary lesion in patients with intracranial ICA occlusions. This may be represented by the fact that 6 out of 7 patients in our pseudodissection group had guide catheters placed proximal to carotid artery bifurcation in anticipation for stent placement for arterial dissection. Merci device was only used in one patient, indicating that preparations were not made in time for the rest of the group since the exact location and type of pathology was not clearly determined upon initial angiography. The phenomenon of pseudodissection has been previously described in coronary literature. Fagan et al suggested that neg- ative contrast streaming from a collateral vessel may be rec- ognized as a dissection in coronary artery.40 Unusual intimal bend has also been viewed as one reason for positive diagno- sis of aortic dissection on high resolution CT angiography.41 This phenomenon should be recognized by interventionalists in order to avoid misdiagnosis and inappropriate therapeutic maneuvers.42 Seven patients in our study had flame-shaped ICA occlusion, highly suggestive of arterial dissection based on our con- ventional knowledge of cerebral angiography. We later found that the pathology was in fact intracranial ICA occlusion, likely from thromboembolism. Upon microcatheter exploration, the inner vascular wall of the vessel at the site of the presumed dissection was intact in all the cases. In our series, we do see a relatively low success rate of recanalization with endovascular therapy. One explanation may bethe delay in treatment strategy to counter the exact pathology, ie, distal occlusion rather than arterial dissection. Second important factor may be location of clot. We observed that location of clot was more commonly in petro-cavernous segment in patients with pseudodissection, whereas ICA terminus was a less common location when com- pared to patients without pseudodissection. This may repre- sent potentially a larger volume clot obstructing the arterial lumen. We hypothesize that pseudodissection may be a flow-related phenomenon. Due to the complete occlusion in the distal ICA, and lack of contrast runoff in posterior communicating artery or ophthalmic artery, a column of blood stagnates in the cervical ICA proximal to the clot. Upon angiography, the contrast tends to stagnate in the carotid bulb and gives the appearance of a “flame”-shaped occlusion. We therefore suggest that if a flame-shaped occlusion of ICA is seen in an acute ischemic stroke case, further careful exploration is warranted. This may include microcatheter ex- ploration to demonstrate whether the dissection is a true intimal tear versus an angiographic artifact. If the inner wall appears intact and the site of occlusion is distal to site of dissection, treat- ment of distal occluded segment should be considered without any further delay in treatment. We acknowledge the limitations of our study. The data are derived from a retrospective review of small number of patients. Practice variations among different physicians may have affected interpretation of angiograms and the treatment strategy for acute ischemic stroke. The strategy for determination of collateral flow varied among physicians and CT angiogram, CT perfusion, and contralateral angiogram was used alone or in combination. Therefore, a standardized evaluation of collateral flow and analysis in our report was limited. Conclusion Pseudodissection is an angiographic phenomenon often ob- served
flow and analysis in our report was limited. Conclusion Pseudodissection is an angiographic phenomenon often ob- served in acute intracranial ICA occlusion. The diagnosis of this phenomenon is made by further exploration of the affected 388 Journal of Neuroimaging Vol 23 No 3 July 2013 segment. If imaging demonstrates that the carotid artery walls are intact at the site of pseudodissection, and the actual site of occlusion is distal to this site, a diagnosis of pseudodissection can be made. Pseudodissection may carry lower recanalization rates and worse clinical outcomes likely related to a larger clot burden. Early recognition may be crucial in establishing an appropriate treatment plan. References 1. IMS Study Investigators. Combined intravenous and intra-arterial recanalization for acute ischemic stroke: the Interventional Man- agement of Stroke Study. Stroke 2004;35:904-911. 2. Furlan A, Higashida R, Wechsler L, et al. 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dissection with tandem internal carotid Siddiq et al: Prognostic Significance of Pseudodissection Phenomenon 389 and middle cerebral artery occlusion. Stroke 2007;38:2270- 2274. 39. Qureshi AI. Acute ischemic stroke. In: Text Book of Interventional Neurology. Cambridge University Press, 2011:69-94. 40. Bonde P, Yuh DD. Intra-aortic intimal band presenting as an aor- tic pseudodissection. J Thorac Cardiovasc Surg 2010;139(4):e64-e65. [Epub 2009 Feb 20]. 41. Garnic JD, Lee DW, Garza JL. Pseudodissection of the coronary artery: a variation caused by interventional tools. Cathet Cardiovasc Diagn 1993;29(4):298-300. 42. Fagan LF Jr, Aguirre FV, Deligonul U, et al. Pseudodissection: negative contrast streaming from collateral flow branch mimicking coronary arterial dissection. Cathet Cardiovasc Diagn 1989;18(1): 15-17. 390 Journal of Neuroimaging Vol 23 No 3 July 2013
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