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REVIEW ARTICLE Kenneth Ouriel, MD, Review Articles Section Editor Free-floating thrombus of the carotid : Literature review and case reports

Ahmad F. Bhatti, MD,a Luis R. Leon, Jr, MD, RVT,b Nicos Labropoulos, MD,c Tara L. Rubinas, MD,d Heron Rodriguez, MD,a Peter G. Kalman, MD,a Michael Schneck, MD,e,f S. Benn Psalms, BSHS,b and Jose Biller, MD,e,f Maywood, Ill; Tucson, Ariz; and Newark, NJ

Background: Free-floating thrombus (FFT) of the carotid artery is an uncommon entity that usually presents as an acute emergency. Management is based on case reports and series because the natural history and optimal treatment are unknown. This study was conducted to systematically review the world literature in an attempt to better understand FFT, its presentation, distribution, management, and outcome. Method: A literature search in all languages was performed of the PubMed database (>1950s) and Medline database (1966-November 2004). All relevant articles were reviewed and their references analyzed in a similar manner for further literature. Cases from the authors’ institutions were reviewed as well. All cases within the reports were individually assessed for inclusion or exclusion. Inclusion required that the FFT originate or anchor within the carotid artery (ie, excluding emboli, arch thrombi with extensions into the carotid artery), be partially occluding (ie, excluding occlusions, “string-sign,” microscopic thrombus), and ideally have an elongated or protrusive morphology, circumferential flow around the distal portion, and cyclical motion with the cardiac cycles. Results: There were 61 reports reviewed, of which 43 contained FFT cases. These reports had 342 cases (including the current series) that were reviewed, of which 145 met our inclusion criteria. A database was created for qualitative and quantitative assessment of all cases. When data were pooled, appropriate statistical analysis was performed. A limitation of the study is that FFT is under-reported and ill defined, which limited the analysis in quantity and quality. In addition, reporting is not uniform, and therefore, significant data were not always present. In attempting to define FFT and include or exclude cases, subjectivity is inherent. Conclusions: FFT is more frequently reported in men than women, with a ratio of nearly 2:1 (P < .0001), and at a younger age than in most patients with carotid disease (P < .0001 when compared with North American Symptomatic Trial, European Carotid Surgery Trial, and Asymptomatic Carotid Surgery Trial). Symptoms are present in 92% of patients. There was a trend for patients with FFT to be hypercoagulable (47% of those serologically tested). The was the most commonly affected (75%), with being the most common associated pathology. Medical and surgical management have both been used, with neither clearly superior to the other. Medical management for stabilizing neurologic deficits has less risk and less benefit than surgical intervention. (J Vasc Surg 2007;45:199-205.)

The natural history of free-floating thrombus (FFT) in artery. Depending on how FFT is defined, the above enti- the carotid circulation of the carotid artery is unknown. ties may be identical, similar, or completely disparate. FFT may encompass several overlapping pathologies with This lack of a unified definition poses difficulty in differing clinical implications. These include intraluminal identification of uniformly comparable clinical trials or even thrombus, embolic thrombus, plaque thrombus, mobile case studies. As such, to design a clinical management thrombus, and total or near total occlusion of the carotid strategy of FFT that is founded on scientific foundations is very challenging. Furthermore, FFT is a particularly diffi- cult problem for the physician because most patients From the Departments of ,a Pathology,d and Neurology,e present with acute neurologic symptoms and it is unclear Loyola University Medical Center; Vascular Surgery Section, Southern whether surgical or medical treatment is superior. Our Arizona Veteran Affairs Health Care System;b Vascular Surgery Section, experience with four patients with FFT in the carotid artery c University of Medicine and Dentistry; and Department of Neurosurgery, is discussed, along with all published cases, in an attempt to Loyola University of Chicago, Stritch School of Medicine.f Competition of interest: none. better describe patient presentation, diagnostic techniques, Correspondence: Ahmad F. Bhatti, MD, RVT, Vascular Surgery Fellow, and clinical management. Department of Surgery, Bldg. 110, Room 3213, Loyola University Med- ical Center, 2160 S First Ave, Maywood, IL 60153-3304 (e-mail: [email protected]). METHODS 0741-5214/$32.00 Copyright © 2007 by The Society for Vascular Surgery. A search was conducted of the literature on the doi:10.1016/j.jvs.2006.09.057 PubMed (Ն1950s) and Medline databases (1966 to No- 199 JOURNAL OF VASCULAR SURGERY 200 Bhatti et al January 2007 vember 2004). The search included, but was not limited to, the terms intraluminal, carotid, floating, mobile, thrombus, and partial and was performed in various combinations. All reports were obtained and reviewed, and all references were checked for further literature on this topic. These addi- tional reports were also obtained and reviewed. If multiple cases were presented within a paper, each case was individ- ually reviewed for inclusion or exclusion. Although it is difficult to define FFT, the ideal defini- tion would be: an elongated thrombus attached to the arterial wall with circumferential blood flow at its distal most aspect with cyclical motion relating to cardiac cycles. Exclusion criteria included cases of FFT from known or probable (according to the authors) embolic sources, com- plete or “string sign” of the carotid artery, small intraplaque thrombi, smooth mural thrombi, thrombi orig- inating outside or not involving the carotid artery, periop- erative thrombi, or insufficiently described thrombi. Fig 1. A color duplex ultrasound scan demonstrates free-floating A database was created to record the following variables thrombus in the internal carotid artery. from the literature review: number of patients, age, sex, presentation, pretreatment diagnostic modalities used, ar- terial segments involved, hypercoagulability, underlying was noted as well. Patients who received any medical man- Յ pathology, medical or surgical treatment, specific treatment agement who also underwent surgical interventions 30 type, 30-day post-treatment neurologic morbidity and all- days of presentation were placed in the surgical manage- cause mortality, and length of follow-up. Patients were ment group. considered symptomatic if they had any transient, evolving, Treatment outcome was recorded for fixed or evolving or fixed neurologic deficit in the territory of the FFT. neurologic deficits. Resolution or cessation of transient Diagnostic modalities were only recorded during the symptoms, such as transient ischemic attacks, was recorded pretreatment phase; follow-up modalities were excluded. as “no change.” Computed tomography (CT) and CT angiograms (CTA) The 30-day mortality after institution of medical or were combined into one group. CT without CTA was only surgical therapy was documented. The length of follow-up Ͻ recorded as a diagnostic modality if the FFT was identified was assigned into one of three categories: 6 months, 6 to Ͼ in the carotid artery on conventional axial images. Mag- 12 months, 12 months. ␹2 netic resonance (MR), MR angiography (MRA), angio- Descriptive statistics were used for analysis. The graphic, and duplex ultrasound (DU) images were similarly analysis was used for analysis of differences in sex distribu- recorded. The involved segment was recorded on the basis tion. The analysis of the age difference between our study of the attachment site of the FFT. and others, as well as between men and women, was Hypercoagulability was recorded as positive or negative performed with unpaired t tests. only if such a diagnostic evaluation was specifically pursued RESULTS or a probable hypercoagulable state such as cancer was clearly documented. The underlying lesion (eg, plaque) of Current series the FFT was recorded. Patient 1. A 41 year-old woman presented with right- Medical treatment was recorded in two categories: sided focal deficits. CT revealed an infarct in the left carotid anticoagulation and antiplatelet therapy. Anticoagulation artery territory. MRA and angiography demonstrated a left was considered to be treatment with heparin, warfarin, or internal carotid artery (ICA) FFT. On further work-up, their equivalents. Antiplatelet therapy was considered to be multiple pulmonary emboli were seen on spiral CT of the treatment with or other agents of similar mechanism chest. Results of evaluations for protein C, protein S, of action. Patients receiving both anticoagulation and an- antithrombin III, C-reactive protein, and anticardiolipin tiplatelet therapy were considered to be part of the antico- antibody were normal, and dilute Russell viper venom time agulation group. The mean duration of anticoagulation was normal. She was placed on warfarin anticoagulation therapy, if available, was recorded. If follow-up studies were therapy and discharged without further events. performed to reassess the FFT on medical treatment, they Patient 2. A 63-year-old woman presented with were recorded in one of three categories: complete disso- speech difficulty and left hand paresthesias. She reported lution, persistence (whether larger or smaller), or occlu- two similar transient episodes in the prior 3 weeks. MR/ sion. MRA revealed an infarct in the right ICA distribution along Surgical treatment was defined as delayed if performed with of the right ICA. DU imaging confirmed this Ͼ7 days after presentation, as some physicians choose to stenosis with an overlying FFT (Fig 1). A carotid endarter- treat with anticoagulation first. The type of surgical therapy ectomy (CEA) was performed Յ24 hours of presentation, JOURNAL OF VASCULAR SURGERY Volume 45, Number 1 Bhatti et al 201 and the patient was discharged uneventfully with no further symptoms. Patient 3. A 76-year-old man underwent a follow-up DU scam after CEA, which showed recurrent stenosis (Ͼ80%) and FFT of the ICA. He was asymptomatic and subsequently underwent surgical intervention for the ste- nosis and FFT. Owing to a previous CEA, the patient underwent a carotid bypass because an endarterectomy could not be performed. His recovery was uneventful and he remained asymptomatic. Patient 4. A 66-year-old man was admitted with new onset of slurred speech and clumsiness of his right hand, which were transient. He had had three similar episodes in the last 4 months, which were initially assumed to be secondary to polymyalgia rheumatica. The CT result was unremarkable. MR/MRA revealed old left-hemispheric in- farcts and a significant stenosis of the left ICA. FFT and high-grade stenosis were demonstrated on subsequent DU imaging. The patient underwent an urgent CEA. Histopa- thology confirmed FFT (Fig 2). Recovery was uneventful, and the patient was discharged symptom-free. Literature search Cases and demographics. In addition to these four patients, 61 articles were found with reports on FFT, and 18 were excluded because they did not meet our inclusion criteria. The remaining 43 articles reported 338 cases, of which 141 met our inclusion criteria. Most of the excluded cases were clearly not related to FFT. Our series added another four patients, bringing the total to 145 (Table).1-44 Most reports consisted of single patients, with the largest series containing 29 patients.45 Gender information was available for 124 patients, of which there were 84 men and 40 women (P Ͻ .0001). Age data were available in 117 patients, who had a mean age of 57.6 Ϯ 13.6 years (range, 28 to 90 years). Men had a mean Fig 2. A, A photograph of the opened carotid endarterectomy age of 58.6 years, and women, 55.8 (NS, P ϭ .45). This was gross specimen demonstrates a pedunculated thrombus extending into the lumen of the vessel. B, A photomicrograph shows the significantly younger than the mean ages in comparative pedunculated thrombus arising from the fibrous cap of an under- patients in the North American Symptomatic Carotid End- lying atheromatous plaque with associated calcification. The arterectomy Trial, European Carotid Surgery Trial, and thrombus shows features of organization (recanalization). (Hema- 46-48 Asymptomatic Carotid Surgery Trial (P Ͻ .0001). toxylin and eosin stain, original magnification ϫ4.) Presentation, imaging, and anatomic distribu- tion. On presentation, 92% (133/145) of patients were symptomatic, 4% (6/145) were asymptomatic, and insuffi- (8/116) each. The external carotid artery (ECA) was only cient information was reported for 4% (6/145). There were reported as being involved in two patients, and in each of 169 pre-treatment radiographic investigations in 145 pa- these, it was an extension of FFT in the carotid artery. tients, of which 84% (122/145) had catheter cerebral Associated pathology. An association of FFT with angiography, 25% (36/145) had DU imaging, 4% had a carotid plaque was reported in 30 of the 44 articles, which MR/MRA, and 3% had CT/CTA. When only one pre- involved the ICA in most cases. An association with carotid treatment diagnostic modality was used, the most common was described in three reports, whereas in the was catheter angiography at 70% (102/140). DU imaging remainder, the association was unknown. was used in 6% (9/145). One patient had CT/CTA, and Hypercoagulability was documented in 16 patients, of no patients had MR/MRA. More than one modality was whom eight were serologically proven, and eight were used in 23% (33/145). estimated to have a hypercoagulable state by the presence Data for segmental distribution in the carotid artery of of associated conditions such as cancer. Hypercoagulability FFT was available in 116 patients. The ICA was the most was serologically excluded in an additional nine patients; common site at 75% (87/116), followed by the common therefore, 47% of patients (8/17) tested serologically were carotid artery (CCA) and the carotid bifurcation in 7% hypercoagulable. The underlying pathology was difficult to JOURNAL OF VASCULAR SURGERY 202 Bhatti et al January 2007

Free-floating thrombus literature with cases meeting to 24 weeks; mean, 9.1 weeks). Follow-up data for radio- inclusion criteria graphic evaluation of the FFT after treatment with antico- agulation was available for 28 of the 33 patients. Complete Author Year Cases (n) FFT cases Language dissolution of the FFT without any neurologic events oc- curred in 24 (86%), with persistence of FFT in two and Ehrenfeld1 1966 44 4 English Hugh2 1970 3 3 English occlusion in two. The 30-day posttreatment outcome was Roberson3 1973 9 9 English available in 35 patients. Of these 20% (7/35) improved, Ojemann4 1975 40 1 English 77% (27/35) had no progression of neurologic symptoms, 5 Goldstone 1976 12 2 English and 3% (1/35) worsened. One death occurred in this Seibert6 1976 1 1 English Yarnell7 1978 3 3 English group, but this was before institution of any treatment. Donnan8 1979 3 2 English There were no post-treatment deaths in the immediate Dunnick9 1979 1 1 English 30-day period. Taber10 1979 1 1 English Surgical treatment and outcome. Ninety-four (65%) 11 Caplan 1984 9 9 English of 145 patients underwent surgical treatment. Of these, six Effeney12 1984 1 1 English Baker13 1985 1 1 English were treated with carotid artery stenting, three with carotid Biller14 1986 9 8 English artery bypass, and the remainder with CEA. Immediate Pelz15 1986 14 13 English surgical intervention (Յ7 days) occurred in 79 (82%) of 96 16 Pessin 1986 5 4 English patients. The remaining 17 were treated with anticoagula- Walters17 1987 64 6 English Arning18 1988 1 1 English tion first for at least 7 days, followed by delayed interven- Gates19/Buchan20 1988 30 29 English tion (3 carotid stents, and 14 CEA). Postoperative (30-day) Kotval21 1989 1 1 English outcome data were available for 70% (67/96) of patients. Combe22 1990 6 6 English Of those who had surgical intervention, 37% (25/67) 23 Cardon 1992 1 1 French improved, 54% (36/67) had no progression of neurologic Chan24 1992 1 1 English Fregonese25 1993 2 2 English symptoms, and 9% (6/67) worsened. There were no deaths Spiegel26 1994 1 1 German in the 30-day postoperative period. Follow-up was reported Stewart27 1994 1 1 English in 58 patients and lasted Ͻ6 months in 21, 6 months to 1 28 Ko 1997 2 2 English year in 14, and Ͼ1 year in 23 patients. Murrle29 1998 1 1 German Szendro30 1999 2 2 English Pauli31 2000 1 1 English Schlachetzki32 2000 1 1 English DISCUSSION Busch33 2002 1 1 English One of the first possible reports on FFT is from Chiari49 34 Cho 2002 1 1 English in 1905, where he describes, on postmortem, an elongated Mathew35 2002 1 1 English Rossetti36 2002 1 1 English 1.5-cm intraluminal thrombus as the probable source of a 50 Silver37 2002 1 1 English patient’s . Gunning et al, in a heavily cited 1963 Chakhtoura38 2003 2 2 English report on a series of “mural thrombosis,” describes clinical 39 Hagiwara 2003 1 1 Japanese vignettes on 16 patients with varying degrees and types of Gonzalez40 2004 3 3 English Gorican41 2004 1 1 Czech intraluminal thrombus. Antemortem clinical and postmor- Greiner42 2004 53 8 English tem pathologic findings are discussed in detail. Many of Sparing43 2004 1 1 English these cases involve small mural thrombi or findings not Longo44 2005 1 1 English definitively FFT. Nonetheless, the cases provide some of Current series 2005 4 4 English the early insight on thrombus in the carotid artery and its Total cases 342 145 link to neurologic disturbances. FFT, Free-floating thrombus. The lack of a unified definition of FFT has led to many reports about this entity containing variable pathophysiol- assess because the information or description of underlying ogy (eg, cardioembolic) that did not meet the inclusion lesions was insufficient. criteria.51-66 These different cases may not be comparable Medical treatment and outcome. Of 145 patients, or have the same etiologic, diagnostic, therapeutic, or medical management was performed in 43 (30%), surgical prognostic implications. Intuitively, the 145 cases reviewed in 94 (65%), and no treatment information was reported in may therefore underestimate the actual incidence. Two eight. Of 43 patients treated medically, 33 (77%) were retrospective studies where consecutive cerebral angio- anticoagulated with or without antiplatelet therapy, nine grams were reviewed suggested an incidence of 0.4% (9/ (21%) received with antiplatelet therapy alone, and one was 2250) and 0.7% (7/1000).3,14 A similar retrospective re- treated with steroids. The latter patient died 5 days after his view with DU imaging of the carotid demonstrated diagnosis. It is not known why this patient was treated with an incidence of 0.05% (1/2000).18 In addition to imaging steroids, but the cause of death was likely the consequence studies, FFT may be misidentified intraoperatively as an of inappropriate therapy. atherosclerotic plaque instead of thrombus, thereby con- The length of anticoagulation treatment was available tributing to the underestimation of the incidence of this in eight patients, and lasted a median of 5 weeks (range, 2 entity. JOURNAL OF VASCULAR SURGERY Volume 45, Number 1 Bhatti et al 203

Almost all of the patients reported in the literature were “middle of the road” option that offers either less risk or symptomatic. The natural history of either symptomatic or less benefit over surgery. asymptomatic patients is not known, although one would One of the more intriguing approaches, performed in a expect it to be adverse in the former. Most patients pre- significant number of patients, was a combined approach. sented with transient neurologic symptoms, were younger Patients were treated with anticoagulation for several weeks than typically seen with atherosclerotic carotid disease, and and then underwent surgical intervention. Also of interest were predominantly male. Although underlying lesions is the incorporation of endovascular techniques that has included carotid aneurysms, small dissections, and athero- emerged in the management of FFT.38,40 Unfortunately, matous plaques, in most cases, the etiology was not clear. owing to the small number of these subtypes of manage- Furthermore, although our data on hypercoagulability ment, no definitive statements can be made about the were limited, our results suggest that this may play a signif- relative risk/benefit. icant role in the pathophysiology of FFT. CONCLUSIONS Angiography was used heavily in the diagnostic phase of FFT. This may reflect the historic bias of obtaining FFT affects men more than women, with a ratio of angiograms for carotid disease, as many of the papers nearly 2:1 at a younger age than most patients with carotid predate the era of DU imaging. When more than one disease. More than 90% of patients presented with neuro- modality was used, findings were congruent, suggesting logic symptoms. All initial diagnostic modalities were con- angiography is not mandatory and that CTA, MRA, or DU gruent, and therefore probably equivalent, in delineation of imaging are sufficient. Despite one case report where a FFT. This may obviate the need for confirmatory studies stroke was precipitated during a DU examination of a FFT, such as cerebral angiography unless otherwise warranted. DU imaging remains the safest and least invasive study.24 There was a trend for patients with FFT to be hypercoag- The dictum of immediately operating on symptomatic ulable. Atherosclerosis was the most common etiology FFT may need to be re-evaluated. Complete dissolution of noted, with the ICA being more frequently involved. Al- the FFT, without any further neurologic progression, oc- though medical and surgical management have both been curred in 86% of patients treated medically. 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