J Neurosurg Pediatrics 7:637–642,
7:000–000, 2011

Balloon-assisted Onyx embolization of cerebral
single-channel pial arteriovenous fistulas
Technical note
C. Benjamin Newman, M.D.,1 Yin C. Hu, M.D., 2 Cameron G. McDougall, M.D., 3
and Felipe C. Albuquerque, M.D. 3
1
Division of Neurosurgery, University of California, San Diego, California; 2Department of Neurosurgery,
Case Western Reserve University Medical Center, Cleveland, Ohio; and 3Division of Neurological Surgery,
Barrow Neurological Institute, St. Joseph’s Hospital and Medical Center, Phoenix, Arizona

Object. Pial arteriovenous fistulas (AVFs) of the brain are rare vascular malformations associated with significant risks of hemorrhage and neurological deficit. Depending on their location and high-flow dynamics, these lesions
can present treatment challenges for both endovascular and open cerebrovascular surgeons. The authors describe a
novel endovascular treatment strategy that was used successfully to treat 2 pediatric patients with a pial AVF, and they
discuss the technical nuances specific to their treatment strategy.
Methods. A single-channel high-flow pial AVF was diagnosed in 2 male patients (6 and 17 years of age). Both
patients were treated with endovascular flow arrest using a highly conformable balloon followed by Onyx infusion
for definitive closure of the fistula.
Results. Neither patient suffered a complication as a result of the procedure. At the 6-month follow-up in both
cases, the simple discontinuation of blood flow had resulted in durable obliteration of the fistula and stable or improved neurological function.
Conclusions. Onyx can be delivered successfully into high-flow lesions after flow arrest to allow a minimally
invasive and durable treatment for pial AVFs. (DOI: 10.3171/2011.4.PEDS10577)

Key Words
•
fistula
pial arteriovenous fistula

•
•

balloon-assisted embolization
•
arteriovenous malformation •
vascular disorder

A

ngiographically, single-channel pial AVFs of the
brain are characterized by an immediate and often
indistinct transition from artery to vein without an
intervening nidus or capillary bed, as occurs in arteriovenous malformations. Pial AVFs can be congenital or
acquired, and they are distinct from dural AVFs in that
their blood supply is derived from cortical or pial arteries.
Moreover, the lesion does not lie within the dural leaflets.
They typically display high-flow dynamics and are frequently associated with large venous varices. Symptoms
attributable to pial AVFs are usually the consequence of
high-flow arteriovenous shunting or mass effect from
the venous varices. Pial AVFs account for 1%–5% of all
brain vascular malformations.3,10,11
The natural history of pial AVFs is unfavorable; the
mortality rate associated with conservative treatment
can be as high as 63%.9 Several investigators have re-

Abbreviations used in this paper: AVF = arteriovenous fistula;
VA = vertebral artery.

J Neurosurg: Pediatrics / Volume 7 / June 2011

ported that resection of these lesions is unnecessary and
that simple flow discontinuation via surgical clipping or
endovascular embolization is a safe and effective treatment.4,12–14 Endovascular embolization is usually preferred for lesions in areas difficult to access surgically;
however, the individual characteristics of a given fistula
can make embolization difficult. We report the novel application of Onyx embolic agent with balloon-assisted
flow arrest in the successful embolization of 2 large intracranial pial AVFs.

Case 1

Illustrative Cases

History and Examination. This 6-year-old boy presented with progressive headaches, lethargy, and the subacute onset of left hemiparesis. Computed tomography
studies of the head showed several large calcified masses
in the posterior fossa and pineal region. The largest mass
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in the posterior fossa obliterated the aqueduct of Sylvius,
and the patient demonstrated early triventricular hydrocephalus and lateral displacement of the brainstem (Fig.
1). Contrast-enhanced MR images characterized the lesion as vascular and prompted consultation with our neurovascular team. The patient underwent cerebral angiography, which demonstrated a single-channel, high-flow
pial AVF with 3 venous varices.

eter into the feeding artery, just proximal to the fistulous
point. A 7 × 7–mm HyperForm balloon (ev3, Inc.) was advanced along the microcatheter and positioned just distal
to the exit of the feeding artery from the VA but proximal

Surgical Technique. Embolization was performed with
neurophysiological monitoring (somatosensory evoked potentials and electroencephalography) while the patient was
under general anesthesia. After bifemoral access was established, the remainder of the procedure was performed
with full anticoagulation. Angiograms were obtained first
via simultaneous injections of the VAs in standard projections so that the relationship of the fistulous point and feeding artery to the vertebrobasilar junction, posterior inferior
cerebellar artery, and anterior inferior cerebellar artery
could be visualized. Downstream of the first giant varix,
venous drainage occurred primarily through the vein of
Galen, which also demonstrated aneurysm dilation (Fig. 2).
After the angioarchitecture of the lesion was delineated, the diagnostic catheter was exchanged for a 6 Fr
guide catheter into the right VA. A 2.4 Fr Echelon microcatheter (ev3, Inc.) was positioned through the guide cath-

Fig. 1. Case 1. Preoperative CT scans (left) and MR images (right)
showing the large venous varices displacing the brainstem and compressing the aqueduct, resulting in obstructive hydrocephalus.

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Fig. 2. Case 1. Preembolization lateral (upper) and posteroanterior
(lower) projections of the right VA injection showing the large aneurysmal dilations of the draining veins, including the vein of Galen. The presence of a stricture in the straight sinus may explain the development
of the alternate drainage pathways through the deep cervical system.

J Neurosurg: Pediatrics / Volume 7 / June 2011

Balloon-assisted embolization of high-flow fistulas
to the microcatheter. The balloon was then carefully inflated, and flow arrest through the fistula was confirmed
with an injection through the right VA guide catheter.
When the balloon was inflated, the working microcatheter was primed with saline and dimethyl sulfoxide in
the standard fashion. Altogether, about 1.4 ml of Onyx 34
(8% ethylene vinyl alcohol; ev3, Inc.) was infused under
continuous fluoroscopic visualization. During embolization the balloon was partially deflated, and repeat angiography through the guide catheter demonstrated some persistent opacification of the varix. The balloon was reinflated,
and the remainder of the Onyx was infused into the cast.
Again, the balloon was slowly deflated, and the Onyx plug
was carefully observed for stability. Angiography studies
repeated through the guide catheter confirmed obliteration
of the fistula. The balloon was reinflated, and the working microcatheter was slowly withdrawn under aspiration.
Note that the microcatheter was withdrawn while the balloon was inflated to minimize the chance of dislodging
the Onyx plug. When the working catheter was removed,
the balloon was deflated and removed. A final angiogram
reconfirmed obliteration of the fistula (Fig. 3). After the
procedure the patient’s anticoagulation was reversed with
intravenous protamine, and manual pressure was applied
to the arteriotomy sites.

Postoperative Course. Follow-up angiography at 8
months (Fig. 4) confirmed a durable result. Magnetic resonance imaging at 6 months (Fig. 5) showed no appreciable
change in the mass effect due to the thrombosed varix with
improvement in his ventriculomegaly. The patient remains
asymptomatic.

Case 2

History and Examination. This 17-year-old boy underwent attempted embolization of a large posterior fossa
pial AVF at another institution 2 years before consultation with our neurovascular team. Initially, the lesion was
discovered after he had suffered a spontaneous hemorrhage that caused substantial neurological deficits, including coma, hemiplegia, and lower cranial neuropathies. In
the ensuing months, the patient made an almost complete
recovery and was left with only deafness in his right ear
at the time of our evaluation. The referring institution had
attempted coil embolization, which failed when the coil
migrated out of the fistulous point and into the venous
pouch (Fig. 6).

Surgical Technique. As in the patient in Case 1, the
procedure was performed with neurophysiological monitoring while the patient was under general anesthesia. After bifemoral arterial access was established, anticoagulation with intravenous heparin was begun. Each VA was
selectively catheterized with a 5 Fr UCSF II diagnostic
catheter. An angiogram of the simultaneous injection of
the VAs was obtained (Fig. 6). We identified the feeding
arterial pedicle to the fistula arising from the right VA.
The arterial segment leading to the fistulous point was
slightly shorter than in the patient in Case 1 and required
a modification of the approach. The diagnostic catheter in
the right VA was then exchanged for a 6 Fr guide catheter.
A 7 × 7–mm HyperForm balloon was advanced over an
J Neurosurg: Pediatrics / Volume 7 / June 2011

Fig. 3. Case 1. Postembolization right VA injection angiogram, posteroanterior projection, confirming obliteration of the fistula.

0.010-in microguidewire and positioned in the right VA
across the ostium of the feeding artery. A 2.4 Fr Echelon
microcatheter was positioned in the feeding artery just
proximal to the fistulous point (identified by the change
in caliber of the artery). The balloon was then inflated in
the VA and allowed to herniate slightly into the feeding
artery (Fig. 7).
An angiogram obtained through the guide catheter
showed that the balloon was occluding the fistula. An
angiogram obtained through the contralateral VA demonstrated adequate perfusion of the posterior circulation.
The working catheter was primed with saline and dimethyl sulfoxide according to the manufacturer’s specifications. Altogether, about 2 ml of Onyx 34 was infused
into the feeding artery. Onyx was noted to cast around the
herniated portion of the balloon, but no reflux into the VA
was seen (Fig. 8).
The balloon was slowly deflated, and the Onyx cast
was thought to be stable. An angiogram obtained through
a guide catheter injection showed that the fistula had been
obliterated. The balloon was reinflated and the working
microcatheter was withdrawn. Final angiography studies obtained after the microcatheter and balloon were removed showed no arteriovenous shunting.
Postoperative Course. Follow-up imaging 6 months
after embolization confirmed that closure of the fistula
was stable (Fig. 9). The patient remains at his neurological baseline.

Discussion

Little is known about the natural history of intracranial pial AVFs given the rarity of these lesions. However,
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Fig. 4. Case 1. Follow-up angiograms, posteroanterior (left) and lateral (right) projections, obtained 8 months after embolization, demonstrating a durable result.

spontaneous closure of the fistula cannot be expected. If
left untreated, these lesions can cause seizures, headache,
hemorrhage, high-output cardiac failure, macrocephaly,
neurological deficit, and symptoms of increased intracranial pressure.1,2,5 Their origin is unknown. Simple flow discontinuation without lesion resection has been shown to be
a safe and effective treatment for pial AVFs. Consequently, endovascular embolization has become the preferred
method of treatment for most pial AVFs. These fistulas are
usually diagnosed during infancy or early childhood, and
most cases are considered to be congenital.6,8
The goal of endovascular embolization should be
obliteration of the fistula with as little embolic material as
possible. High-flow lesions can make it difficult to deliver
the desired embolic agent precisely to the fistulous point.
Delivery of embolic material into the draining vein can
compromise venous outflow of the fistula or cause pulmonary embolus. Restricted venous outflow in the setting of
an incompletely obliterated fistula can have disastrous consequences.
Balloons have been used successfully to modulate
flow through high-flow AVFs and malformations. As far
as we know, however, this is the first report on the successful embolization of giant, high-flow AVFs with Onyx.
Some authors have advised against using nonadherent
embolic agents, such as Onyx, to treat fistulous lesions.7
But we have found that the increased ability to control the
delivery of Onyx, as compared with N-butyl cyanoacrylate, allows more precise targeting and delivery of embolic material to the fistulous point. The ability to modulate
or arrest flow through a large artery using highly flexible
and navigable balloons augments this degree of precision.
Coil embolization with balloon flow arrest has been
successfully used in the treatment of single-channel highflow fistulas in the past. However, published success rates
for endovascular techniques have not been impressive. In
their series of 79 patients, Hoh et al.4 reported that the
failure rate of endovascular embolization for pial AVFs
was as high as 40%. Given the fact that attempted coil
embolization had already failed in the patient in Case 2,
we were compelled to try a different treatment modality.
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The patient in Case 1 may have also had a good outcome with coil embolization; however, we believed that
the segment of artery leading to the fistula would easily
accommodate an Onyx cast and would be favorable for
this approach. In our opinion, Onyx infusion after flow
arrest offers an additional level of control as compared
with coil embolization. Even with balloon-assisted flow
arrest, coil loops can frequently herniate distally into the
venous pouch. Our treatment goal is to obliterate the fistula with as little embolic material as possible, and we be-

Fig. 5. Case 1. Axial MR image obtained at 6 months, demonstrating
no progression of the varix, stable mass effect, and improvement in
ventriculomegaly.

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Balloon-assisted embolization of high-flow fistulas

Fig. 6. Case 2. Angiogram, posteroanterior projection, demonstrating simultaneous injections of the VA. Note the presence of the coil
mass within the varix from the prior embolization attempt.

lieve that the additional level of control afforded by Onyx
deposition helps us to achieve this objective. Nonetheless,
coil embolization remains a viable treatment option, and
decisions about specific technique should be made based
on the individual patient characteristics and the comfort
level of the surgeon.

Fig. 7. Case 2. Subtracted roadmap radiograph obtained after balloon inflation, showing the conformable balloon herniating into the
feeding artery of the fistula. The Onyx cast (white arrow) can be seen
between the portion of the balloon herniating into the vessel (white arrowhead) and the orphaned coil mass (black arrow).

J Neurosurg: Pediatrics / Volume 7 / June 2011

Fig. 8. Case 2. Postembolization angiogram confirming obliteration
of the fistula.

Even with newly available microcatheters and balloons, a comment about the techniques used in these cases
is warranted. It is our practice to use full anticoagulation in
elective cases in which a balloon is utilized, to minimize
the chance of thromboembolic complications. The most
critical portion of the procedure is deciding when to deflate
the balloon after the initial cast of Onyx has been delivered
to the fistulous point. In both of our cases, we undertook
a series of inflation-deflation cycles between infusions of
Onyx to continually assess for stability. If the cast is not
stable, venous embolization can ensue after flow resumes.
Slow, patient, and meticulous injection at the initial appearance of Onyx at the microcatheter tip provides a maximally viscous and controllable cast with which to work. If the
balloon actually occludes the feeding artery, the risk of the
Onyx plug migrating should be minimal.
The goal should be radial expansion of the cast. Antegrade progression of the embolic agent into the venous
pouch should be avoided, unless the geometry of the ensu-

Fig. 9. Case 2. Posttreatment MR image (left) and MR angiogram
(right) showing thrombosis of the varix and closure of the fistulous
point.

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ing cast would be favorable to prevent distal embolization
(that is, V- or L-type configuration). Reflux around the
distal end of the balloon is not altogether undesirable, but
excessive embolic agent around the microcatheter should
be avoided. We tend to allow more time than usual for the
Onyx cast to solidify between injections (compared with
embolization for a low-flow lesion) and are slightly more
aggressive in infusing to try to radially appose the cast
to the walls of the artery. We recommend removing the
microcatheter with the balloon inflated to minimize the
chance of disrupting the cast.
Thrombosis of the varix can lead to a temporary exacerbation of mass effect. Hydrocephalus as a result of
venous occlusion has also been reported.6 We believe that
the risk of this complication can be reduced by applying the Onyx cast precisely at the fistulous point and taking care not to allow the embolic agent to progress into
the normal venous circulation. Both of our patients were
hospitalized for 72 hours of observation after their procedures and treated with prophylactic dexamethasone.
The two featured cases demonstrate the novel application of balloon-assisted Onyx closure of high-flow
pial AVFs, with successful and durable obliteration of the
target lesions and no distal embolization of the embolic
material.
Disclosure
The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this
paper.
Author contributions to the study and manuscript preparation include the following. Conception and design: Albuquerque,
McDougall. Acquisition of data: all authors. Analysis and interpretation of data: Albuquerque, Newman, Hu. Drafting the article:
Newman. Critically revising the article: Albuquerque, Newman, Hu.
References
1. Aoki N, Sakai T, Oikawa A: Intracranial arteriovenous fistula
manifesting as progressive neurological deterioration in an infant: case report. Neurosurgery 28:619–623, 1991
2. García-Mónaco R, Taylor W, Rodesch G, Alvarez H, Burrows
P, Coubes P, et al: Pial arteriovenous fistula in children as presenting manifestation of Rendu-Osler-Weber disease. Neuroradiology 37:60–64, 1995
3. Halbach VV, Higashida RT, Hieshima GB, Hardin CW, Dowd

642

CF, Barnwell SL: Transarterial occlusion of solitary intracerebral arteriovenous fistulas. AJNR Am J Neuroradiol 10:
747–752, 1989
4. Hoh BL, Putman CM, Budzik RF, Ogilvy CS: Surgical and
endovascular flow disconnection of intracranial pial singlechannel arteriovenous fistulae. Neurosurgery 49:1351–1364,
2001
5. Lasjaunias P: A revised concept of the congenital nature of
cerebral arteriovenous malformations. Interv Neuroradiol 3:
275–281, 1997
6. Lv X, Jiang C, Li Y, Yang X, Wu Z: Clinical outcomes of
endovascular treatment for intracranial pial arteriovenous fistulas. World Neurosurg 73:385–390, 2010
7. Mounayer C, Hammami N, Piotin M, Spelle L, Benndorf G,
Kessler I, et al: Nidal embolization of brain arteriovenous
malformations using Onyx in 94 patients. AJNR Am J Neuroradiol 28:518–523, 2007
8. Nakiri GS, Abud TG, Oliveira RS, Santos AC, Machado HR,
Abud DG: Endovascular treatment of intracranial pial arteriovenous fistula. Arq Neuropsiquiatr 68:463–465, 2010
9. Nelson PK, Niimi Y, Lasjaunias P, Berenstein A: Endovascular embolization of congenital intracranial pial arteriovenous
fistulas. Neuroimaging Clin N Am 2:309–317, 1992
10. Tomlinson FH, Rüfenacht DA, Sundt TM Jr, Nichols DA,
Fode NC: Arteriovenous fistulas of the brain and the spinal
cord. J Neurosurg 79:16–27, 1993
11. Viñuela F, Fox AJ, Kan S, Drake CG: Balloon occlusion of a
spontaneous fistula of the posterior inferior cerebellar artery.
Case report. J Neurosurg 58:287–290, 1983
12. Weon YC, Yoshida Y, Sachet M, Mahadevan J, Alvarez H,
Rodesch G, et al: Supratentorial cerebral arteriovenous fistulas (AVFs) in children: review of 41 cases with 63 non choroidal single-hole AVFs. Acta Neurochir (Wien) 147:17–31,
2005
13. Yoshida Y, Weon YC, Sachet M, Mahadevan J, Alvarez H,
Rodesch G, et al: Posterior cranial fossa single-hole arteriovenous fistulae in children: 14 consecutive cases. Neuroradiology 46:474–481, 2004
14. Youn SW, Han MH, Kwon BJ, Kang HS, Chang HW, Kim
BS: Coil-based endovascular treatment of single-hole cerebral
arteriovenous fistulae: experiences in 11 patients. World Neurosurg 73:2–10, 2010
Manuscript submitted December 20, 2010.
Accepted April 1, 2011.
Address correspondence to: Felipe C. Albuquerque, M.D., c/o
Neuroscience Publications, Barrow Neurological Institute, St.
Joseph’s Hospital and Medical Center, 350 W. Thomas Road, Phoenix, Arizona 85013. email: neuropub@chw.edu.

J Neurosurg: Pediatrics / Volume 7 / June 2011