Peer-Review Short Reports

Intravascular Ultrasound in the Evaluation and Management of Cerebral

Venous Disease

Maxim Mokin1,5, Peter Kan2,6, Adib A. Abla2,6, Tareq Kass-Hout1,5, Kenneth V. Snyder2-4,6, Elad I. Levy2-4,6,Adnan H. Siddiqui2-4,6

-BACKGROUND: Intravascular ultrasound (IVUS) is an important diagnostictool in many interventions, particularly coronary and carotid artery angioplastyand stenting. In contrast, its application in the management of diseases of thecerebral venous system remains an unexplored territory. We report threepatients in whom IVUS was used during angiography for the evaluation ofvenous flow obstruction secondary to venous sinus thrombosis, venous sinusstenosis, and a transverse sinus mass lesion, respectively. In addition, wereview current literature to summarize previous experience, focusing on theadvantages and limitations of IVUS technology in interventional cardiology,carotid artery disease, and venous disease.

-CASE DESCRIPTIONS: In all three cases, IVUS was used without anycomplications and provided critical information that guided further managementof these distinct diseases. IVUS helped diagnose the presence of intraluminalthrombus, severe stenosis, and a mass lesion in the transverse sinuses and alsohelped assess the response to angioplasty of the stenotic regions.

-CONCLUSIONS: IVUS is a promising tool that has potential to improve diag-nostic accuracy and to guide the management of several diseases of thecerebral venous system. The cases we describe suggest that IVUS can besuccessfully used when performing endovascular interventions in patients withobstruction of venous outflow secondary to venous sinus stenosis, thrombosis,or mass lesions.

Key words- Cerebral venous stenosis- Cerebral venous thrombosis- Intravascular ultrasound imaging- Venous flow obstruction

Abbreviations and AcronymsCT: Computed tomographyDSA: Digital subtraction angiographyIVUS: Intravascular ultrasoundMRI: Magnetic resonance imaging

From the Departments of 1Neurology,2Neurosurgery, and 3Radiology, and 4Toshiba

Stroke Research Center, School of Medicine and BiomedicalSciences, University at Buffalo, State University of NewYork, Buffalo; and the Departments of 5Neurology and6Neurosurgery, Gates Vascular Institute, Kaleida Health,Buffalo, New York, USA

To whom correspondence should be addressed:Adnan H. Siddiqui, M.D., Ph.D.[E mail: asiddiqui@ubns.com]

Citation: World Neurosurg. (2013) 80, 5:655.e7 655.e13.http://dx.doi.org/10.1016/j.wneu.2012.04.004

Journal homepage: www.WORLDNEUROSURGERY.org

Available online: www.sciencedirect.com

1878 8750/$ see front matter ª 2013 Elsevier Inc.

INTRODUCTION

Intravascular ultrasonography is animportant diagnostic tool for intravascularinterventions. In cardiology, intravascularultrasound (IVUS) is predominantly usedfor the evaluation of coronary disease. It iscapable of detecting early atheroscleroticdisease as well as assessing furtherprogression and regression of atheroscle-rosis and providing accurate measure-ments. IVUS is commonly used as anadjunct to percutaneous coronary inter-ventions (3, 9) and provides high-resolu-tion vascular images, more recentlymaking it an attractive tool for the evalu-ation of cerebrovascular disease, such ascarotid artery angioplasty and stenting(8, 22). The value of IVUS in the diagnosisand treatment of the venous system is lessestablished; in the venous system, it ismainly used in the treatment of iliac andfemoral vein disease (13, 14). Here, we

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present our early experience in applyingIVUS for the evaluation and treatment ofcerebral venous disease, including a caseof venous sinus thrombosis, a case ofvenous sinus stenosis in the setting ofbenign intracranial hypertension, anda case of an obstructive mass in a venoussinus. In addition, we provide a review ofcurrent literature discussing the advancesand limitations of IVUS in facilitating thediagnosis of cerebrovascular disease.

CASE DESCRIPTIONS

Case 1: Venous Sinus ThrombosisA 23-year-old man with a history ofpulmonary embolism and deep-veinthrombosis secondary to lupus anticoag-ulant syndrome presented to the emer-gency department at our hospital witha new-onset headache. A computed

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tomography (CT) venogram revealedevidence of intraluminal thrombus withinthe superior sagittal sinus, extending tothe torcula and into the right transversesinus (Figure 1A). The left transverse sinusappeared hypoplastic, although a smallthrombus could not be excluded on thebasis of this image. The patient wastreated with a continuous intravenousheparin infusion for a total of 9 days anddischarged home on warfarin.He returned to the emergency depart-

ment 3 weeks later, complaining of wors-ening headache and blurry vision. Thistime, the physical examination revealedbilateral papilledema, and a repeat CTvenogram revealed significant improve-ment of flow in the superior sagittal sinus;however, there was a residual filling defectin the right transverse sinus, possiblysecondary to the presence of intraluminalthrombus versus structural stenosis.

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Figure 1. Case 1. Computed tomography venogram demonstrates extensive filling defect throughoutthe superior sagittal sinus and in the right transverse sinus, suggesting thrombosis of thesestructures (A). The left transverse sinus appears hypoplastic, although the presence of a smallthrombus cannot be excluded. Venous phase of a digital subtraction angiogram demonstratesnear complete resolution of the thrombus inside the superior sagittal sinus but a persistent fillingdefect suspicious for thrombus is present in the transverse sinus bilaterally (B).

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Digital subtraction angiography (DSA) wasperformed to further investigate thedegree of venous sinus thrombosis andshowed a filling defect suspicious forpersistent thrombus in the transversesinus bilaterally (Figure 1B).Using a right femoral vein access

approach, we advanced a 6-French Raabecatheter (Cook Medical, Bloomington,Indiana, USA) into the right internal jugularvein. A tapered Glidewire Gold microwire(Radiofocus, Terumo, Tokyo, Japan) wasused to navigate a Nautica microcatheter(ev3/Covidien Vascular Therapies, Mans-field, Massachusetts, USA) into the lefttransverse sinus. The microwire was thenexchanged for a balance middleweight wire(Abbott Vascular, Abbott Park, Illinois,USA), and a 3.5-French 20-MHz Eagle EyeIVUS probe transducer (Volcano Thera-peutics, Rancho Cordova, California, USA)was delivered into the left transverse sinus.IVUS recording was started in the left

transverse sinus, then continued into thetorcula, and finally through the righttransverse sinus. It showed a very stenoticleft transverse sinus as well as a thrombuspresent in the right transverse sinus(Figure 2). The IVUS probe was removed,and a 4 � 40-mm Aviator balloon (CordisVascular, Bridgewater, New Jersey, USA)was brought up into the left transversesinus for a series of angioplasties. It wasthen exchanged for a 6 � 40-mm Aviatorballoon and, starting distally in the left

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transverse sinus and moving the balloonproximally towards the torcula, anotherseries of angioplasties was performed,followed by angioplasty of the right trans-verse sinus, up to the level of the righttransverse-sigmoid junction (Figure 3A).The IVUS probe was brought up again andanother recording was obtained, beginningin the left transverse sinus, proceedingthrough the torcula, and ending in the righttransverse sinus, showing improved diam-eter of both transverse sinuses witha persistent thrombus within the righttransverse sinus (Figure 3B and C). Thepatient had an uncomplicated post-operative course and was discharged homeon warfarin.

Case 2: Venous Sinus StenosisA 27-year-old woman with a history ofbenign intracranial hypertension presentedwith worsening headache and blurry vision.Despite a long-term course of medicaltreatment with acetazolamide and top-iramate, as well as serial lumbar punctures,her headaches had continued to worsen,and a neurologic examination performed atthe time revealed severe papilledema. CTvenography showed bilateral transversesinus stenosis, and the patient underwentangiography for further evaluation of thedegree of stenosis and possible stenting.Diagnostic angiography confirmed severetransverse sinus stenosis bilaterally(Figure 4A). Then, using a similar approach

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as in Case 1, via femoral vein access, weadvanced a Nautica microcatheter into theleft jugular vein through the right jugularvein, the right transverse sinus, the torcula,and the left transverse sinus, respectively.The patient underwent multiple angio-plasty attempts of the right and left trans-verse sinuses with a 3.5 � 15-mm Sprinterballoon (Medtronic, Inc, Minneapolis,Minnesota, USA), which did not show anysignificant improvement of the degree ofstenosis. IVUS recording confirmed thepresence of persistent stenosis of thetransverse sinus bilaterally (Figure 4B). Thetorcula region had normal anatomicalappearance (Figure 4C).Angioplasty was then attempted with

a 6 � 40-mm EverCross balloon (ev3/Covidien Vascular Therapies) but wasunsuccessful because the lesion could notbe crossed. The patient began to complainof worsening headache, and the procedurewas terminated. The next day, with thepatient under general anesthesia,successful stenting of the right transverseand the right sigmoid sinuses wasaccomplished with a 7 � 40-mm Precisestent (Cordis). Subsequently, the patient’sheadaches improved significantly.

Case 3: Compressive Mass Lesion in theTransverse SinusesAn 8-year-old boy with new-onset head-ache and blurry vision was found to havesignificant papilledema on physicalexamination. The magnetic resonanceimaging (MRI) results were suspicious foran extra-axial mass lesion that waspossibly obstructing the superior sagittaland right transverse sinuses (Figure 5);a lumbar puncture confirmed an elevationof intracranial pressure (55 cm). Anangiogram was performed to evaluate thedegree of venous sinus flow obstruction.Using the right femoral vein accessapproach, we advanced a Neuron catheter(Penumbra Inc., Alameda, California, USA)over a 0.035-inch Glidewire (Terumo,Somerset, New Jersey, USA) to the righttransverse sinus. A Prowler-Plus micro-catheter (Cordis) was advanced overa microwire into the left transverse sinus.Diagnostic angiographic runs revealeda round filling defect in the right transversesinus, close to the torcula. Using a balancemiddleweight wire, we advanced the IVUSprobe into the left transverse sinus anda recording was obtained, which

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Figure 2. Case 1. Images A and B were obtained by intravascular ultrasound (IVUS) probe positionedin the right transverse sinus. The grey circle in the middle of the images represents the 3.5 FrenchIVUS transducer. Horizontal and vertical axis tracings are 1 mm apart. Cross sectional IVUS image (A)demonstrates the presence of a dark echodense region between the 1 o’clock and 5 o’clock position,indicating thrombus. Another cross sectional view shows severe stenosis in the right transversesinus, measuring approximately 2 � 4 mm (B), with significant flow obstruction. Longitudinalreconstruction view (C) shows irregular shape of the transverse sinus bilaterally, with several distinctareas demonstrating the presence of thrombus and stenosis. The white horizontal bar within thetransverse sinus represents the position of the IVUS transducer. Area of large diameter in the middleis the torcula.

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demonstrate a large round hyperechoicmass inside the right transverse sinus,located close to the torcula (Figure 6). AnAlligator retrieval device (ChestnutMedical, Menlo Park, California, USA) wasadvanced into the right transverse sinuswith the Prowler-Plus microcatheter andthe microwire to obtain a biopsy samplefrom the lesion. Unfortunately, this stepwas not successful because the mass wasmobile and the endovascular graspers wereunable to hold on to the tissue for biopsy.More aggressive tools were not usedbecause of the intracranial location of themass and risk of sinus wall disruption. Wefurther attempted angioplasty of the righttransverse to sagittal sinus; however,inflation of the balloon simply displacedthe mass but did not affect the luminalnarrowing; therefore, the procedure wasterminated.The case was discussed at our multidis-

ciplinary conference; an open surgicalexploration of the torcula would carry

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significant risk; therefore, the patient wasfollowed closely by a neurosurgeon anda neuro-ophthalmologist. The differentialdiagnosis included arachnoid granulations,cavernoma, or meningioma. On radio-graphic follow-up, there has been noapparent change in the appearance of thelesion, and the patient has demonstratedimproving vision and resolution ofpapilledema.

DISCUSSION

In recent years, IVUS has become a valuabletool in cerebrovascular interventions,including carotid artery angioplasty andstenting (4, 8). In contrast, clinical appli-cation of IVUS in the management of cere-bral venous disease remains an unexploredterritory. For instance, the most recentguidelines on the management of cerebralvenous thrombosis do not include IVUS inthe list of diagnostic tools (16). Unlike thearterial system, in which the association

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between the degree of carotid arterystenosis and changes in blood flowdynamics is well established (7), there is atpresent no established threshold for thedegree of venous stenosis that is consideredhemodynamically significant because ofthe great variability of the anatomy of thecerebral venous system.Similarly, no ultimate diagnostic test

currently exists to reliably assess hemo-dynamics of the venous system in bothhealthy patients and in those experiencingpathological states, such as venous sinusstenosis and thrombosis. Transcranialduplex ultrasound is a noninvasiveapproach that has been studied in initialdiagnosis and follow-up assessment oftreatment response in patients withvenous sinus thrombosis. Unfortunately,this tool has significant limitations indiagnostic sensitivity and accuracy;normal venous blood flow velocities oftendo not exclude the diagnosis of venousthrombus, when confirmed by angiog-raphy that demonstrates thrombosis of thecerebral veins (21). With the use of echocontrast agents, transcranial color-codedduplex ultrasound can enhance detectionof thrombus by demonstrating a fillingdefect. However, even such an approachprovides poor visualization of significantcomponents of the cerebral venous system,such as portions of the superior sagittal,transverse, and straight sinuses, whencompared with magnetic resonance angi-ography (18, 19) because of the difficulty ofobtaining transosseous windows that allowadequate ultrasonic visualization.The incorporation of IVUS as a diag-

nostic modality for evaluation of cerebralvenous disease offers several potentialbenefits, such as high-resolution cross-sectional images providing informationabout the structure and thickness of thevessel wall, as well as composition of thelesion of interest (such as homogeneousversus heterogeneous appearance andpresence of calcified lesions). In carotidartery disease management, IVUS hasdemonstrated excellent ability in detectingintimal thickenings, plaque ulcerations,and calcifications (10, 11).Magnetic resonance venography is

commonly used for diagnostic purposes,given its noninvasive approach and lack ofradiation exposure. However, it canprovide false results, such as flow gapsthat can be mistaken for thrombus when

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Figure 3. Case 1. Digital subtraction angiogram revealing balloon angioplasty of the left transversesinus (A). The balloon has been brought up and inflated inside the left transverse sinus.Cross sectional intravascular ultrasound view (B) demonstrates partial resolution of stenosis of thebilateral transverse sinuses after balloon angioplasty. As seen on the longitudinal view (C), there issignificant improvement in the degree of stenosis; however, some areas still show focal narrowing ofthe vessel wall attributable to persistent thrombus.

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one is evaluating vessels with very slow orturbulent flow patterns, as the result ofanatomical variation, such as the trans-verse sinuses (24). In one study, transverse

Figure 4. Case 2. Venous phase of a digital subtractiodemonstrates poor filling of bilateral transverse sinuspresence of severe stenosis, more prominent on theCross sectional intravascular ultrasound (IVUS) view osinus (B) shows severe stenosis. Virtually no flow is

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sinus flow gaps were observed in as manyas 31% of nondominant transverse sinusesin healthy control subjects (2). AlthoughDSA is the “gold standard” for diagnostic

n angiogram (A)es, indicating theright than left side.f the right transverseseen between the

IVUS probe (grey circle) andstenotic area measures appappearance of the torcula r6 � 10 mm.

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evaluation, it is also an endoluminalmodality and often has the same problemsin differentiating thrombus from structuralstenosis. DSA provides no information onthe wall and adjacent structures, such aschronic intraluminal thrombus versushypoplastic sinus, which is where IVUS hasbeen incredibly helpful.An example of both diagnostic and

intraprocedural use of IVUS comes fromthe treatment of chronic venous insuffi-ciency of lower extremities, where IVUShas been extensively used to assist inplacement of venous stents (14, 15, 17).When evaluating chronic iliac veinobstruction, IVUS demonstrates excellentdetection of fine intraluminal and muralcomponents, including the presence ofpostthrombotic trabeculations, intra-luminal webs, and external compression,which was found to be superior to contrastvenography (15). Also, compared withvenography, IVUS is more accurate inestimating the degree and extent of iliacvein stenosis—the information that iscritical for the selection of proper dimen-sions of balloons and stents for endovas-cular interventions (15). Similarly, IVUSshows superiority in thrombus detectionwhen compared with angioscopic evalua-tion of saphenous and iliac veins (17).Mural thrombus is characterized by a dark(echodense) appearance, and its detectioncan be further enhanced by the use ofcolor-flow IVUS technology (6, 11).

the walls of the right transverse sinus. Theroximately 2 � 2 mm. For comparison, normalegion is shown (C), measuring approximately

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Figure 5. Case 3. Magnetic resonanceimaging, fluid attenuated inversion recoverysequence, axial view, shows an ovalhyperintense lesion near the torcula region.No focal edema is seen. On the basis ofappearance, it is difficult to accuratelydetermine whether the lesion is locatedwithin the right transverse sinus,immediately adjacent to the right transversesinus, or connected to the right occipital pole.

Figure 6. Case 3. Intravascular ultrasound cross sectional view (A) shows a large mass between the8 o’clock and 1 o’clock position. The appearance of the mass is highly echogenic and homogeneous.No calcifications or heterogeneous regions are seen. For comparison, the normal appearance of theright transverse sinus is shown (B). The lumen of the sinus is patent and shows uniform blood flow.Longitudinal reconstruction view (C) demonstrates that the large mass lesion is located within theright transverse sinus, causing focal flow obstruction.

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After venous angioplasty and stenting,IVUS can be successfully used to accuratelyestimate response to interventions ormonitor the degree of restenosis, includingproviding information on precise locationand morphology of the stenotic segmentand identification of in-stent thrombus. Inour series, cases 1 and 2 each provide anexample of IVUS offering important detailsof anatomical characteristics of areas ofstenosis and thrombosis of the venoussinus, helping determine whether addi-tional treatment was required.In case 1, on the basis of the appearance

of the cerebral venous sinus on repeatDSA, we could not accurately establishwhether the filling defect we observedwithin both the right and left transversesinuses was attributable to thrombus orstructural stenosis. IVUS clearly demon-strated a focal echodense lesion within theright transverse sinus, confirming thepresence of persistent thrombus in theright transverse sinus and distinguishing itfrom anatomical stenosis, which was seenin the left transverse sinus. By using IVUS,we were able to accurately estimate thedegree of stenosis of the left transversesinus and a repeat IVUS recordingconfirmed that balloon angioplasty wassuccessful in treating the stenosis and nofurther interventions were necessary.

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In case 2, IVUS demonstrated persistentstenosis, despite repeat balloon angioplastyattempts, which guided our team of inter-ventionists to further perform stenting.Cross-sectional IVUS images providea scale bar allowing the real-timemeasurement of vessel diameter in bothvertical and horizontal axes. By the use ofthis scale bar, a fast and accuratemeasurement of response to venousangioplasty or stenting can be performedduring the procedure by comparing IVUSrecordings immediately pre- and poststentdeployment.Case 3 illustrates how IVUS demon-

strated the homogeneous hyperechoicnature of the lesion and confirmed itsintravascular location. Despite obtainingan MRI study, it was difficult to differen-tiate intra-axial versus extra-axial locationof the mass lesion. The IVUS recordingclearly showed that the mass was locatedwithin the lumen of the right transversesinus and likely adjacent to the vesselwalls. This information was critical indetermining the differential diagnosis and

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choosing observation instead of an inva-sive surgical debulking approach. Thesethree cases provide examples of howadditional information obtained by IVUShelped establish accurate diagnoses andguide us in determining the appropriatetreatment strategies.An additional advantage of IVUS is that it

does not require the administration ofa radiographic contrast agent, which allowsmultiple recording passes during interven-tional procedures in patients with renalfailure, such as evaluation of the degree ofstenosis pre- and postangioplasty andstenting, thus minimizing the amount ofcontrast agent used and the risk for wors-ening of renal function. The use of IVUShasalready been demonstrated to be cost-effective when used in percutaneous car-diologic interventions; the increase ininitial procedural costs associated with theuse of IVUS is outweighed by the reductionof costs associated with rehospitalizationand revascularization procedures (12).Once IVUS becomes a more widely usedtool in management of cerebral venous

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system disease, it will be of interest todetermine whether it has similar cost-effective potential.IVUS can potentially be performed

parallel to another diagnostic approach,namely, cerebral venous pressuremeasurement, which is recorded atvarious locations within the cerebralvenous sinus system by the use of a pres-sure transducer. Measuring venous pres-sure before and after angioplasty andstenting in cases of benign intracranialhypertension refractory to medical treat-ment demonstrated dramatic reduction invenous pressure after intervention (1). Thisapproach provides quantitative informa-tion about the pressure profiles inside thecerebral venous system.Several limitations should be

mentioned in conjunction with consider-ations to include IVUS as a diagnostic tool.Given the prominent tortuosity of theintracranial venous circulation and thelimited flexibility of the IVUS catheter andits relatively large diameter, distal veinsoften cannot be accessed for recording.However, the venous system predomi-nantly consists of vessels with largediameters and less resistance, whencompared with the arterial system, whichallows the examination of most intracra-nial cerebral veins, including the trans-verse, sigmoid, and superior sagittalsinuses. In several studies authors havedemonstrated the safety of IVUS whenevaluating extracranial and intracranialportions of the carotid arterial system, aswell as the posterior circulation, includingthe vertebral arteries (4, 5, 20, 23). In thesetting of cerebral venous thrombosis,there is a risk to dislodge a thrombuswhile navigating the IVUS transducer.However, unlike in the arterial systemwhere thrombus disruption can result inthe occlusion of distal arterial branchesand cause an embolic stroke, a thrombusoriginating in the venous system will betrapped by the lung capillaries, thus pre-venting it from embolizing to the cerebralarterial circulation.

CONCLUSIONS

IVUS is a promising tool that has potentialto improve diagnostic accuracy and toguide the management of several diseasesof the cerebral venous system. The caseswe describe suggest that IVUS can be

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successfully used when performing endo-vascular interventions in patients withobstruction of venous outflow secondaryto venous sinus stenosis, thrombosis, ormass lesions. Previous experience withIVUS technology in the treatment ofcoronary and carotid artery disease canhelp increase its clinical application inother areas of cerebrovascular diseases.

ACKNOWLEDGMENTS

The authors thank Paul H. Dressel, BFA,for preparation of the illustrations andDebra J. Zimmer, AAS CMA-A, for edito-rial assistance.

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Conflict of interest statement: E. I. Levy receives researchgrant support (principal investigator: Stent-AssistedRecanalization in acute Ischemic Stroke, SARIS), otherresearch support (devices), and honoraria from BostonScientific* and research support from Codman & Shurtleff,Inc. and ev3/Covidien Vascular Therapies; has ownershipinterests in Intratech Medical Ltd. and Mynx/Access Closure;serves as a consultant on the board of Scientific Advisors toCodman & Shurtleff, Inc.; serves as a consultant per projectand/or per hour for Codman & Shurtleff, Inc., ev3/CovidienVascular Therapies, and TheraSyn Sensors, Inc.; and receivesfees for carotid stent training from Abbott Vascular and ev3/Covidien Vascular Therapies. E. I. Levy receives no consultingsalary arrangements. All consulting is per project and/or per

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hour. (*Boston Scientific’s neurovascular business has beenacquired by Stryker.). T. Kass-Hout has received grantsupport from Genentech. A. H. Siddiqui has receivedresearch grants from the National Institutes of Health (co-investigator: NINDS 1R01NS064592-01A1, Hemodynamicinduction of pathologic remodeling leading to intracranialaneurysms) and the University at Buffalo (ResearchDevelopment Award); holds financial interests in Hotspur,Intratech Medical, StimSox, and Valor Medical; serves asa consultant to Codman & Shurtleff, Inc., ConcentricMedical, ev3/Covidien Vascular Therapies, GuidePoint GlobalConsulting, and Penumbra; belongs to the speakers’ bureausof Codman & Shurtleff, Inc. and Genentech; serves on anadvisory board for Codman & Shurtleff; and has receivedhonoraria from Abbott Vascular, American Association ofNeurological Surgeons’ courses, an emergency medicineconference, Genentech, Neocure Group LLC, an EmergencyMedicine Conference, Annual Peripheral Angioplasty and AllThat Jazz Course and from Abbott Vascular and Codman &Shurtleff, Inc. for training other neurointerventionists incarotid stenting and for training physicians in endovascularstenting for aneurysms. A. H. Siddiqui receives no consulting

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salary arrangements. All consulting is per project and/or perhour. K. V. Snyder serves as a consultant to, a member of thespeakers’ bureau, and has received honoraria from Toshiba.He serves as a member of the speakers’ bureau for ev3 andThe Stroke Group (consultants to the health care industry,Littleton CO) and has received honoraria from these entities.The remaining authors have no conflicts to report. Theinstitutional review board at the University at Buffalo, StateUniversity of New York (Buffalo, New York, USA) approvedthis study (HSIRB Project #NEU3380811E), and a standardHealth Insurance Portability and Accountability Act-compliant protocol was followed.

Received 11 October 2011; accepted 3 April 2012

Citation: World Neurosurg. (2013) 80, 5:655.e7-655.e13.http://dx.doi.org/10.1016/j.wneu.2012.04.004

Journal homepage: www.WORLDNEUROSURGERY.org

Available online: www.sciencedirect.com

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