Transarterial Onyx Embolization of Bilateral Transverse–Sigmoid Dural Arteriovenous Malformation with Transvenous Balloon Assist—Initial U.S. Experience with Copernic RC Venous Remodeling Balloon

Transarterial Onyx Embolization of Bilateral Transverse–Sigmoid Dural Arteriovenous Malformation with Transvenous Balloon Assist—Initial U.S. Experience with Copernic RC Venous Remodeling Balloon

Accepted Manuscript ® Transarterial Onyx Embolization of Bilateral Transverse–Sigmoid Dural Arteriovenous Malformation with Transvenous Balloon Assist...

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Accepted Manuscript ® Transarterial Onyx Embolization of Bilateral Transverse–Sigmoid Dural Arteriovenous Malformation with Transvenous Balloon Assist - Initial US Experience with the Copernic RC Venous Remodeling Balloon Abdulrahman Alturki, MBBS, MSc, FRCSC, Alejandro Enriquez-Marulanda, M.D., Philip Schmalz, M.D., Christopher S. Ogilvy, M.D., Ajith J. Thomas, M.D. PII:

S1878-8750(17)31811-9

DOI:

10.1016/j.wneu.2017.10.083

Reference:

WNEU 6736

To appear in:

World Neurosurgery

Received Date: 13 September 2017 Revised Date:

13 October 2017

Accepted Date: 14 October 2017

Please cite this article as: Alturki A, Enriquez-Marulanda A, Schmalz P, Ogilvy CS, Thomas AJ, ® Transarterial Onyx Embolization of Bilateral Transverse–Sigmoid Dural Arteriovenous Malformation with Transvenous Balloon Assist - Initial US Experience with the Copernic RC Venous Remodeling Balloon, World Neurosurgery (2017), doi: 10.1016/j.wneu.2017.10.083. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

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Transarterial Onyx® Embolization of Bilateral Transverse–Sigmoid Dural Arteriovenous Malformation with Transvenous Balloon Assist -- Initial US Experience with the Copernic RC Venous Remodeling Balloon

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Abdulrahman Alturki, MBBS, MSc, FRCSC1,2 *, Alejandro Enriquez-Marulanda, M.D.1 *, Philip

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Schmalz M.D.1,3, Christopher S. Ogilvy, M.D.1, Ajith J. Thomas, M.D. 1

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Neurosurgical Service, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston,

MA, USA 2Department of Neurosurgery, The National Neuroscience Institute, King Fahad Medical

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City, Riyadh, Saudi Arabia. 3Department of Neurosurgery, University of Alabama, Birmingham,

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AL, USA.

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*These authors contributed equally to this study.

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Keywords: Dural arteriovenous fistulas; Therapeutic embolization; balloon-assisted technique;

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sinus protection; Meningeal arteries; Intracranial pressure; Balloon occlusion; Dimethyl sulfoxide;

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Tantalum

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Running Head: Balloon-assisted protection during Onyx embolization.

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Corresponding Author

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Ajith J. Thomas, M.D.

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Neurosurgical Service

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Beth Israel Deaconess Medical Center

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Harvard Medical School

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110 Francis Street

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Boston, MA, 02215

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Email: [email protected]

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Phone: 617-632-9785

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Introduction

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Dural-Arterio-venous-fistulas(DAVFs) consists of anomalous connections between

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branches of dural arteries to dural venous sinuses, dural veins, meningeal veins or cortical

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veins1. These vascular lesions account for approximately 15% of arteriovenous

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malformation and most commonly involve the transverse and the sigmoid sinus2–4. DAVFs

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can be asymptomatic but also can be associated with either intracranial hemorrhage

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(especially when there is cortical venous drainage and cortical reflux), venous hypertension

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and non-hemorrhagic neurologic deficits1–3.

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Treatment options for DAVF include observation, microsurgery, stereotactic radiosurgery,

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vascular embolization or a combination of these modalities4–6. Currently, the mainstay of

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treatment for DAVFs involves endovascular approaches, especially for high-grade lesions

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that are associated with higher risks of complications1. Low-grade lesions may be

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considered for endovascular treatment if associated with bothersome symptoms, such as

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intractable tinnitus or headaches.

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Transarterial embolization with preservation of the venous sinus has become the preferred

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approach due to the development of newer liquid embolic agents such as Onyx®(ev3

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Endovascular, Plymouth, MN)7. Onyx® is a non-adhesive agent that polymerizes gradually

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in contact with blood that allows controllable penetration, high occlusion rates and low

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procedure-related complications8. Because of its ability to enter small vessels, it is

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important to be attentive to progression and migration of Onyx®, especially when

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potentially dangerous anastomoses are present8. Two significant drawbacks with Onyx® are

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the possibility of arterial reflux alongside the delivery microcatheter and inadvertent venous

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penetration beyond the venous side of the fistula, even compromising the lumen of the

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venous sinuses9.

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For further precision and avoidance of venous sinus compromise and sacrifice during

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embolization, the use of a temporary balloon occlusion to protect the patency of dural

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sinuses from embolic agents migration have been described in few publications outside the

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US4,4–7,9–13. Here we present a case of bilateral symptomatic Borden Type II and Cognard

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type IIB DAVF treated successfully with transarterial Onyx® embolization with

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transvenous balloon protection of the sinus. This case is the first reported use of the

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Copernic® RC balloon(BALT Extrusion, Montmorency, France) in the United States under

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the “compassionate use” guidelines of the FDA.

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Materials and methods

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Case description

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A 64-year-old man, with past medical history of hypertension, dyslipidemia, renal cell

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carcinoma(in remission) and a former smoker, presented with bilateral pulsatile tinnitus and

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visual decline.

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On exam, he was found to have bilateral papilledema. Radiologic evaluation consisting of

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an MRI and MRA of the brain and a diagnostic cerebral angiogram demonstrated a

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complex bilateral type 2 dural arteriovenous fistula with feeding vessels from bilateral

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occipital and middle meningeal, left ascending cervical, bilateral marginal tentorial arteries,

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and posterior meningeal branch of the right vertebral artery(Figure 1). Retrograde venous

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reflux through the superior sagittal sinus was noted. The principal venous drainage from

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the brain was through enlarged scalp and superficial veins rather than the dural venous

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sinuses, indicating venous hypertension.

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After multidisciplinary team discussion and review of available literature, treatment was

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offered. Surgical strategy consisted of transarterial Onyx® embolization with venous sinus

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balloon-assisted protection technique since both transverse sinus and sagittal sinus was

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involved in drainage of the fistula.

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Following IRB approval, we obtained "compassionate use" FDA approval of the Copernic®

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RC balloon for one time use to repair this DAVF.

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Endovascular treatment technique

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Treatment was carried out endovascularly under general anesthesia in a staged fashion. The

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second session was delayed one week to observe for deficits and allow for patient recovery.

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Via transfemoral arterial access, the right posterior division of the middle meningeal

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artery(MMA)

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microcatheter(MicroVention, Tustin, CA, USA) through a 6F Benchmark(Penumbra,

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Alameda, CA) guiding catheter in the ECA. Transfemoral venous access was also

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established and the Copernic® RC 10x80mm balloon was positioned in the right transverse-

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sigmoid sinus across the torcula into the left transverse sinus. The balloon was inflated

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during embolization to protect the right transverse sigmoid venous sinus system and

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torcula(Figure 2). After creating satisfactory cast in the MMA distribution, the balloon was

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pulled back into the right transverse sigmoid sinus and catheterization of the right occipital

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artery with a double lumen Scepter XC 4x11mm balloon(MicroVention, Tustin, CA, USA)

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was performed(Figure 3). Onyx® was then delivered through the working lumen of the

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inflated arterial balloon until distal penetration was judged sufficient with the Copernic®

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RC balloon inflated during the embolization session. There was a venous pouch in parallel

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to the sigmoid sinus which had fistulous communications from the ascending pharyngeal

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artery which drained into the jugular vein(Figure 3B). This anatomical variant has been

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described in previous studies14. We elected not to embolize this component since the risk of

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cranial nerve deficit would have been high.

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The patient was observed overnight and after an unremarkable hospital course, was

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discharged on postoperative day one.

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In the second stage, the Copernic® RC 10x80mm balloon was positioned in the left

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sigmoid-transverse system through the right internal jugular vein due to difficult left sided

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venous access to the dural sinuses. The balloon was again inflated to protect the left

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transverse sigmoid venous sinus system and torcula during embolization. The left occipital

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artery was catheterized with a double lumen Scepter XC 4x11mm.

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Complete obliteration of the left DAVF was achieved and patency of the left transverse and

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sigmoid sinuses was preserved(Figure 4B&C).

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sigmoid sinus was also conserved post-procedure(Figure 4A&C). The patient recovered

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overnight without signs of neurologic deficit and was again released on postoperative day

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one.

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Patency of the right transverse and

Discussion

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Previous approaches to endovascular treatment of DAVFs involved venous occlusive

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strategies such as coil embolization of the involved dural venous sinus. This deconstructive

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approach risks worsening venous hypertension due to inadequate cerebral venous drainage,

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particularly in the setting of inadequate contralateral venous sinus drainage4,5. The strategy

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of venous sinus occlusion may also cause new lesion formation due to compromised

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venous drainage.5,15

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With improved endovascular devices, approaches which preserve venous drainage have

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been advocated4. Transvenous balloon-assisted transarterial Onyx® embolization for

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DAVFs was first described by Shi et al. in 200911. This case demonstrated safe occlusion of

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DAVF via transarterial means with preservation of the venous sinuses using transvenous

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balloons.

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Transvenous balloon occlusion facilitates embolization by both protecting the patency of

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the venous sinus as well as allowing liquid embolic infiltration into otherwise inaccessible

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meningeal vessels contributing to the fistula.6,9,11. This technique may also decrease the

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number of embolization sessions and improve the chance of anatomical cure11.

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Additionally, transvenous balloon assistance can reduce the amount of embolic agent

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required.6.

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The Copernic® RC Venous Remodeling Balloon, was selected for this case. This is a low-

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pressure, compliant hydrophilic balloon. The balloon is DMSO-compatible and has a

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diameter of up to 10x80mm6. Designed for use with a 6F guide catheter and is designed for

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use with the Trascend 0.014 microwire(Boston scientific, Miami, FL); though in this case a

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Synchro2 Standard wire was used without difficulty. Reports using other devices have

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shown incomplete sinus occlusion and consequent off-target embolization5.

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The MMA has been described as the gateway for successful embolization of these

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lesions.3,5,13 Transverse sinus DAVFs are commonly fed by branches from the middle and

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posterior meningeal artery, by meningeal branches from the ascending pharyngeal artery,

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and by transosseous branches of the occipital artery or, more rarely, of the superficial

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temporal artery10. It is essential that meticulous fluoroscopic monitoring during Onyx®

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injection is performed to be aware of any possible reflux or migration of the embolic

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agent11. Also, for further reduction of the risk of migration into the parent artery, the use of

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a transarterial dual-lumen complement balloon poses the advantage that the inflation of the

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balloon in the feeder vessels avoids the need of a proximal Onyx® plug to prevent the

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reflux9,10, giving an additional safeguard during the procedure.

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One of the major concerns of transvenous balloon-assisted-technique is the pressure

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changes within the intracranial venous drainage when the balloon is inflated, which might

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cause intracranial hypertension or venous territory infarctions6. A balloon inflation test may

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be performed before embolization to assess venous compromise4,6. In cases of embolization

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involving a dominant venous sinus the balloon may be periodically deflated to reduce the

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risk of venous infarction4,6. Systemic heparinization should also be considered to minimize

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the risk of thrombosis of the dural sinus6.

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Risk of Onyx migration to a parallel venous channel is also possible when it is not

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adequately protected by the venous balloon.

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described a case in which migration of Onyx was evidenced in a patient with a Borden type

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II fistula into the proximal vein of Labbé despite the use of venous balloon protection. The

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intervention, however, was stopped timely and no impairment of the patency of the vein

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was noted13. In our case there was evidence of a parallel venous channel of the right

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sigmoid sinus which had fistulous communications from the ascending pharyngeal artery

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which drained into the jugular vein. We elected to not embolize this component due to the

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risk of cranial nerve deficit.

In the series of Piechowiak et al. they

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Conclusions

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Transvenous and transarterial balloon-assisted transarterial Onyx® embolization is

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becoming a useful treatment alternative in selected cases of DAVFs. Previous reports in

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Asia and Europe with venous remodeling balloons are encouraging. We report the first

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known experience with this device in USA. The device performed as expected and there

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were no complications attributable to the device. Additionally, it provided a valuable

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adjunct to improve the safety and efficacy of transarterial embolization. References

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1.

Gandhi D, Chen J, Pearl M, Huang J, Gemmete JJ, Kathuria S. Intracranial dural arteriovenous fistulas: classification, imaging findings, and treatment. AJNR Am J Neuroradiol. 2012;33(6):1007-1013. doi:10.3174/ajnr.A2798.

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2.

Kwon BJ, Han MH, Kang H-S, Chang K-H. MR imaging findings of intracranial dural arteriovenous fistulas: relations with venous drainage patterns. AJNR Am J Neuroradiol. 2005;26(10):2500-2507.

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Griessenauer CJ, He L, Salem M, Chua MH, Ogilvy CS, Thomas AJ. Middle meningeal artery: Gateway for effective transarterial Onyx embolization of dural arteriovenous fistulas. Clin Anat N Y N. 2016;29(6):718-728. doi:10.1002/ca.22733.

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4.

Choi BJ, Lee TH, Kim CW, Choi CH. Reconstructive treatment using a stent graft for a dural arteriovenous fistula of the transverse sinus in the case of hypoplasia of the contralateral venous sinuses: technical case report. Neurosurgery. 2009;65(5):E994996; discussion E996. doi:10.1227/01.NEU.0000351772.45417.92.

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Zhang Y, Li Q, Huang Q-H. Embolization of a superior sagittal sinus dural arteriovenous fistula under intrasinus balloon protection: A case report. Interv Neuroradiol J Peritherapeutic Neuroradiol Surg Proced Relat Neurosci. 2015;21(1):94-100. doi:10.1177/INR-2014-10098.

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Jittapiromsak P, Ikka L, Benachour N, Spelle L, Moret J. Transvenous balloonassisted transarterial Onyx embolization of transverse-sigmoid dural arteriovenous malformation. Neuroradiology. 2013;55(3):345-350. doi:10.1007/s00234-012-1107-8. Pop R, Manisor M, Wolff V, et al. Balloon protection of the Labbé vein during transarterial embolization of a dural arterio-venous fistula. Interv Neuroradiol. 2015;21(6):728-732. doi:10.1177/1591019915609119.

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Saeed Kilani M, Izaaryene J, Cohen F, et al. Ethylene vinyl alcohol copolymer (Onyx®) in peripheral interventional radiology: Indications, advantages and limitations. Diagn Interv Imaging. 2015;96(4):319-326. doi:10.1016/j.diii.2014.11.030.

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Chiu AHY, Aw G, Wenderoth JD. Double-lumen arterial balloon catheter technique for Onyx embolization of dural arteriovenous fistulas: initial experience. J Neurointerventional Surg. 2014;6(5):400-403. doi:10.1136/neurintsurg-2013-010768.

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10. Clarençon F, Di Maria F, Gabrieli J, et al. Double-lumen balloon for Onyx® embolization via extracranial arteries in transverse sigmoid dural arteriovenous fistulas: initial experience. Acta Neurochir (Wien). 2016;158(10):1917-1923. doi:10.1007/s00701-016-2906-1.

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11. Shi Z-S, Loh Y, Duckwiler GR, Jahan R, Viñuela F. Balloon-assisted transarterial embolization of intracranial dural arteriovenous fistulas. J Neurosurg. 2009;110(5):921-928. doi:10.3171/2008.10.JNS08119.

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12. Ponomarjova S, Iosif C, Mendes G a. C, Mounayer C. Endovascular Treatment of Transverse-Sigmoid Sinus Type I Dural Arteriovenous Shunts with Sinus Preservation for Patients with Intolerable Symptoms: Four Case Reports. Clin Neuroradiol. 2015;25(3):313-316. doi:10.1007/s00062-014-0343-1.

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13. Piechowiak E, Zibold F, Dobrocky T, et al. Endovascular Treatment of Dural Arteriovenous Fistulas of the Transverse and Sigmoid Sinuses Using Transarterial Balloon-Assisted Embolization Combined with Transvenous Balloon Protection of the Venous Sinus. AJNR Am J Neuroradiol. 2017;38(10):1984-1989. doi:10.3174/ajnr.A5333.

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14. Caragine LP, Halbach VV, Dowd CF, Ng PP, Higashida RT. Parallel venous channel as the recipient pouch in transverse/sigmoid sinus dural fistulae. Neurosurgery. 2003;53(6):1261-1266-1267.

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15. Kubo M, Kuwayama N, Hirashima Y, Kurimoto M, Takaku A, Endo S. Dural Arteriovenous Fistulae Developing at Different Locations after Resolution of Previous Fistulae: Report of Three Cases and Review of the Literature. Am J Neuroradiol. 2002;23(5):787-789.

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FIGURE LEGENDS:

Figure 1. Preoperative images that evidence bilateral DVFAs. A. Right external carotid artery lateral. B. Right common carotid artery lateral. C. Left external carotid artery lateral. D. Left common carotid artery lateral. E. Right external carotid artery anteroposterior. F. Right common carotid artery anteroposterior. G. Left external carotid artery anteroposterior. H. Left common carotid artery anteroposterior.

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Figure 2. Procedure images that show the Copernic RC balloon inflated in the sinuses. A. Antero-posterior DSA shows deflated and inflated Copernic RC balloon in the right transverse and sigmoid sinus. B. Lateral DSA shows deflated and inflated Copernic RC balloon in the right transverse and sigmoid sinus. C. Right antero-posterior and lateral DSA showing inflated Copernic RC balloon during Onyx® embolization. D. Onyx® cast post- embolization with the inflated Copernic RC balloon.

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Figure 3. Post-procedure images that show obliteration of the feeders. A. AP right common carotid artery B. Lateral right common carotid artery. C. AP left common carotid artery D. Lateral left common carotid artery. E. Onyx® cast after the first procedure. F. Onyx® cast after the second procedure.

Figure 4. Post-procedure images Show Venous Drainage of the Sinuses. A. Lateral DSA in venous phase of right TS and SG sinuses, and IJV showing adequate patency. B. Lateral DSA in venous phase of left TS and SG sinuses, and IJV showing adequate patency. C. AP DSA in venous phase showing bilateral patency of venous sinus drainage.

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Highlights Previous endovascular treatment of DAVF involved venous occlusive strategies. Transvenous balloon occlusion aids embolization by protecting the venous sinus. Transvenous balloon assistance can reduce the amount of embolic agent required

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Abbreviations: Dural Arterio-venous fistulas (DAVFs), Middle Meningeal Artery (MMA), internal

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jugular vein (IJV), External Carotid Artery (ECA), Common Carotid Artery (CCA).