J Neurosurg Pediatrics 12:344–350, 2013

©AANS, 2013

An institutional series and literature review of pial

arteriovenous fistulas in the pediatric population
Clinical article

Peter J. Madsen, M.D., M.B.E.,1 Shih-Shan Lang, M.D.,1

Jared M. Pisapia, M.D., M.T.R.,1 Phillip B. Storm, M.D.,1,3 Robert W. Hurst, M.D., 2
and Gregory G. Heuer, M.D., Ph.D.1,3

Departments of 1Neurosurgery and 2Radiology, Hospital of the University of Pennsylvania; and 3Division of
Neurosurgery, Children’s Hospital of Philadelphia, Pennsylvania

Object. Pial arteriovenous fistulas (PAVFs) are a rare form of cerebrovascular disease that tend to be overrepre-
sented in the pediatric population. There have been limited studies of the clinical features and outcomes in this group
of patients. Here, the authors attempt to better delineate this clinical entity with institutional cases and a review of
the literature.
Methods. A retrospective review of cases at our institution was performed to identify all pediatric patients treated
for a PAVF between 2000 and 2012.
Results. Five patients treated for a PAVF were identified. Patients had a mean age of 1.9 years at diagnosis,
and the most common presenting symptoms were seizure and macrocephaly. Patients were treated primarily with
embolization, and 3 patients required both N-butyl cyanoacrylate (NBCA) glue and coiling. Four of the patients had
complete obliteration of the PAVF and had a pediatric overall performance category score of either 1 (n = 3) or 2 (n
= 1) at follow-up. There was 1 death due to heart failure. Analysis of the literature review suggested that a younger
age or presence of intracerebral hemorrhage (ICH) or congestive heart failure (CHF) at presentation likely predicts
a worse prognosis. Older patients presented more often with ICH, whereas younger patients presented significantly
more often in CHF. The majority of pediatric patients reported on in the literature were treated with endovascular em-
bolization, most commonly with NBCA glue alone. Most patients (65.4%) in the literature had an excellent outcome
without neurological deficit.
Conclusions. Pial AVFs represent a serious yet rare form of cerebrovascular disease. Pediatric patients with ICH
or CHF at presentation or those who are very young are likely to have a worse prognosis. Endovascular management
of these patients has greatly changed the natural history of this disease, but the complication and mortality rates sug-
gest the need for continued insights and advances in treatment.
(http://thejns.org/doi/abs/10.3171/2013.6.PEDS13110)

Key Words      •      pial arteriovenous fistula      •      AVF      •      varix      •      surgery      •     

embolization      •      pediatric      •      vascular disorders

P
ial (or nongalenic) arteriovenous fistulas are a rare
form of cerebrovascular disease consisting of a
high-flow connection between one or more pial ar-
teries and the venous circulation.18,48,53 They are typically
classified as a subtype of pial AVMs, yet are differenti-
ated by their lack of an intervening nidus between the
arterial feeder(s) and venous drainage.24 Pial AVFs have
been found to account for 4.7% of pial AVMs;47 however,
they tend to be overrepresented in the pediatric popula-
Abbreviations used in this paper: AVM = arteriovenous malfor-
mation; CHF = congestive heart failure; CN = cranial nerve; GDC =
Guglielmi Detachable Coil; ICH = intracerebral hemorrhage; MCA
= middle cerebral artery; NBCA = N-butyl cyanoacrylate; PAVF =
pial arteriovenous fistula; PCA = posterior cerebral artery.
tion at an increased incidence of 17.2% of pial AVMs.52
The clinical features of PAVFs, especially in children,
have been described in limited detail in the literature due
to the rarity of this entity. It has been suggested that there
is an increased incidence of venous varices, a higher rate
of seizures, and a lower rate of hemorrhage in children
than in adults.53
The management strategies for PAVFs have under-
gone considerable evolution with the advancement and
refinement of endovascular techniques. Despite advances
in treatment, PAVFs remain a potentially life-threatening
condition, necessitating further evaluation and investiga-
tion. In this study, we identify and delineate the clinical
course of pediatric patients with PAVFs at our tertiary
care children’s hospital. In addition, because of the rarity

344 J Neurosurg: Pediatrics / Volume 12 / October 2013

Pial arteriovenous fistulas in the pediatric population
of pediatric PAVFs, we performed a literature review of
published cases.
Methods
Study Design and Clinical Data
A retrospective review of cases at a single tertiary
referral children’s hospital was performed to identify
patients who demonstrated angiographic evidence of a
PAVF between 2000 and 2012. Patients older than 18
years and those with an isolated AVM or vein of Galen
malformation were excluded. Patient demographics, clin-
ical presentation, radiographic images, angioarchitecture,
treatment details, complications, and outcomes were ex-
tracted from inpatient hospital records and neurosurgical
outpatient clinic charts. Only patients with angiographic
features of a PAVF such as rapid venous filling, large ar-
terial feeder(s), and direct filling of a venous varix were
included. Neurological outcomes were assessed using the
pediatric overall performance category.11,12
Literature Review
We performed a MEDLINE and a Cochrane data-
base search of articles published in the English-language
literature before December 2012 containing the terms
“pial arteriovenous fistula” and “nongalenic arterio-
venous fistula.” We supplemented our search using the
“Related Citations” feature of PubMed and performing
manual reviews of the bibliographies of selected articles.
Only studies in which individual patient data could be
clearly extracted were included in our review. Patients
with AVMs, vein of Galen malformations, or with unclear
angiographic characterization were excluded.
Results
Summary of Cases
Between 2000 and 2012, 5 patients were identified as
meeting our inclusion criteria for a PAVF (Tables 1 and
2). Individual patient cases are described.
Case 1. This 3-month-old boy, who was previously
reported on in the literature,45 presented with evidence of
right CN III palsy, emesis, and a cranial bruit. Magnetic
resonance imaging and MR angiography and convention-
al cerebral angiography demonstrated a large (6.6 × 4.4 ×
4.7–cm) dilation of the M2 branch of the right MCA, caus-
ing mass effect on the midbrain, pons, and CN III. There
was direct communication of this dilation with enlarged
venous drainage into the junction of the right transverse
and sigmoid sinuses.
Embolization of the fistula was performed using
GDCs and NBCA glue, achieving minimal residual fill-
ing. The procedure was complicated by ischemic stroke
of the right MCA territory, resulting in mild hemipare-
sis. At 1 year of follow-up, complete occlusion of the fis-
tula was achieved. The patient’s hemiparesis improved;
however, he ultimately required medial and lateral rectus
muscle resection to correct persistent CN III dysfunction.
Case 2. This 9-month-old boy with seizures, increas-
J Neurosurg: Pediatrics / Volume 12 / October 2013
ing head circumference, and delay of motor development
was found to have angiographic evidence of a mixed
AVM and PAVF with venous varix fed by the right angu-
lar artery that drained into the right sigmoid sinus. Em-
bolization of both the AVM and PAVF was performed
using NBCA glue and resulted in complete occlusion.
The residual nidus of the AVM was resected. There were
no complications from either procedure, and the patient
remained in excellent condition and seizure free during 4
years of follow-up.
Case 3. This 6-month-old boy who presented with
atonic seizures and macrocephaly was found on CT to
have a thrombosed varix. Magnetic resonance angiog-
raphy, MR venography, and cerebral angiography con-
firmed the presence of an occipital PAVF fed by the right
MCA and draining into the straight and right transverse
sinuses via the vein of Labbé (Fig. 1A–C). Embolization
of the fistula was performed using detachable coils and
NBCA glue, with postembolization angiography showing
minimal flow through the PAVF. Radiographic follow-up
over the next 3 months demonstrated complete oblitera-
tion of the fistula (Fig. 1D). After the procedure, the pa-
tient neglected stimuli presented in his left visual field,
but this finding resolved over 3 months. At 3 years follow-
up the patient was neurologically stable and seizure free.
Case 4. This 1-week-old girl presented with CHF and
associated pulmonary hypertension. Magnetic resonance
imaging, MR angiography, MR venography, and cerebral
angiography demonstrated a large PAVF adjacent to the
midbrain comprising numerous dilated arterial feed-
ers arising from the right posterior choroidal artery and
right posterior inferior cerebellar artery with drainage to
the deep cerebral veins. The malformation was associ-
ated with mild hydrocephalus. An attempt at emboliza-
tion was performed using NBCA and detachable coils
with incomplete obliteration and residual arterial feeding
vessels. Postembolization ultrasonography of the head
showed evidence of a possible thalamic infarct. The pa-
tient’s heart failure continued to worsen, and she died at 3
weeks of age of multisystem organ failure.
Case 5. This 8-year-old girl was found to have a
left parietooccipital vascular anomaly on MRI during
workup for multiple cutaneous hemangiomas present
since birth. Genetic testing uncovered a RASA1 muta-
tion passed along by her father who harbored the same
mutation. RASA1-related disorders are characterized by
face and appendicular capillary malformations as well
as AVMs and/or AVFs in the skin, muscle, bone, spine,
and brain.10 The patient was neurologically asymptomatic
from the vascular lesion. On cerebral angiography, she
was noted to have a multichannel PAVF that was fed by
the left pericallosal and posterior cerebral arteries and
drained via the straight sinus with an associated venous
varix (Fig. 2A–C). Embolization was performed using
multiple GDCs, with the achievement of immediate com-
plete obliteration (Fig. 2D). The patient had no complica-
tions from the procedure and continued to be neurologi-
cally intact at 1 month of follow-up.
345
 P. J. Madsen et al.
TABLE 1: Patient characteristics*

Case
No. Age at Dx, Sex Presentation Location Feeding Vessel Draining Vessel Varix
1 3 mos, M CN III palsy, cranial bruit, rt frontotemporal M2 branch of MCA rt transverse sinus yes
 emesis
2 9 mos, M seizure, macrocephaly, rt temporoparietal rt MCA rt sigmoid sinus yes
  developmental delay
3 6 mos, M seizure, macrocephaly rt occipital rt MCA rt vein of Labbé yes
4 1 wk, F heart failure, pulmonary interpeduncular fossa rt posterior choroidal deep cerebral yes
 HTN   artery, rt PICA  veins
5 8 yrs, F cutaneous hemangiomas lt parietooccipital lt pericallosal artery, straight sinus yes
lt PCA

*  Dx = diagnosis; HTN = hypertension; PICA = posterior inferior cerebellar artery.

Literature Review
Sixty-two papers were reviewed; 40 of which were
considered suitable for the current study.1–9,13–17,20–23,26–28,
30–33,35–38,40–44,50–52,54–56
These studies included 27 case re-
ports or series and 13 retrospective studies and yielded
extractable data on 147 cases of intracranial PAVF in pa-
tients younger than 18 years old (Table 3). The mean age of
patients in the literature was 5.02 years with a slight male
predominance, and the most common presenting symp-
tom was seizure, followed by CHF. The most common
first-line treatment modality performed was embolization
with NBCA glue, and the vast majority of patients had no
complications and excellent neurological outcomes.
Discussion
Pial AVF is a rare form of cerebrovascular disease,
with a reported incidence of 3%–7.3% in clinical series of
AVMs in all age groups.40 This increases to a reportedly
higher incidence of 17.2% of AVMs in the pediatric popu-
lation.52 Limited distinction has been made between the
clinical features of this disease in pediatric and adult pa-
tients. To better define the pathogenesis, clinical elements,
therapeutic strategies, and outcomes of this disease in the
pediatric population, we describe our experience with
this clinical entity at our tertiary care children’s hospital
TABLE 2: Treatment and patient outcomes*
and interpret the data reported from our literature review
of pediatric PAVFs.
Clinical Presentation
Similar to vein of Galen aneurysmal malformations,
the clinical presentation in pediatric patients with PAVFs
tends to vary by age. Studies have suggested that neonates
with a PAVF are more likely to present in CHF than older
patients.18,40 This is further supported by the fact that 22
of the 28 patients in our literature review who presented
with cardiac failure were in the neonatal period (< 28
days). The average age of patients presenting in CHF was
0.21 ± 0.52 years compared with 6.2 ± 5.4 years for those
patients presenting without CHF (p < 0.0001, unpaired t-
test). Our series also supported this association, as our pa-
tient who presented with CHF was only 1 week old (Table
1). The other 4 patients were all 3 months of age or older
and did not have symptoms of heart failure. Historically,
newborns with CHF due to a cranial arteriovenous shunt
have a very poor prognosis that approached 100%, but
advances in endovascular techniques in this population
have improved outcomes significantly.13,40
Intracerebral hemorrhage at presentation is also sug-
gested to be age dependent, in that it is typically seen as
a presenting sign in older patients, especially those older
than 15 years.53 In our literature review, the mean age of
patients presenting with ICH was 6.4 ± 5.5 years versus a

Case Embolization Outcome Follow-Up

No. Treatment Modality Material Complication Fistula Occlusion (POPC)† (yrs)
1 embol NBCA, GDCs MCA territory infarct, mild 100% 2 0.9
 hemiparesis
2 embol, op‡ NBCA none 100% 1 4.2
3 embol NBCA, GDCs transient visual field neglect 100% 1 2.8
4 embol NBCA, GDCs thalamic infarct incomplete 6 NA
5 embol GDCs none 100% 1 0.1

*  embol = embolization; NA = not applicable; POPC = pediatric overall performance category.

†  Based on the system of Fiser11 and Fiser and colleagues:12 1 = good overall performance, 2 = mild overall disability, 6 = brain
death.
‡  Surgery was performed only on the nidal portion of the patient’s associated AVM.

346 J Neurosurg: Pediatrics / Volume 12 / October 2013

Pial arteriovenous fistulas in the pediatric population
Fig. 1.  Case 3. Preembolization lateral (A) and anteroposterior (B)
digital subtraction angiograms and MR angiogram (C) showing a right
temporooccipital PAVF arising from an enlarged, distal MCA branch
with deep (vein of Labbé) and superficial drainage and an associated
venous varix. Postembolization MR angiogram (D) demonstrating oblit-
eration of the PAVF.
mean of 4.8 ± 5.4 years for those patients presenting with-
out ICH (p = 0.19, unpaired t-test), although this finding
was not statistically significant.
Treatment of PAVFs
The vast majority of pediatric patients with PAVF in
the literature were treated with endovascular embolization
(113 patients [83.7%]) rather than surgical intervention (23
patients [17.0%]) (Table 3). Of the 23 reports involving sur-
gical interventions, 19 of these cases were reported prior to
2002, which represents a significant shift in management
strategies with the advancement of the endovascular field.
In terms of the type of embolic material used, NBCA glue
alone was the most common (53 [46.9%] of 113) followed
by coiling alone (26 [23.0%] of 113) and combined coil-
ing and NBCA glue (21 [18.6%] of 113; Table 3). Of the
108 patients who underwent embolization as their initial
treatment and had data reported on fistula obliteration, 74
(68.5%) had angiographic evidence of complete oblitera-
tion of their PAVF.
Of the 34 patients who continued to have residual
filling of the PAVF, 24 (70.6%) had initially received
NBCA glue alone, 7 (20.6%) received coiling and NBCA
glue, 2 (5.9%) received coiling alone, and 1 (2.9%) re-
ceived balloon occlusion. In our series, all patients were
treated with endovascular embolization, with one patient
subsequently undergoing open resection of an associated
AVM (Table 2). Three of the patients from our institu-
tional series required combined embolization material
J Neurosurg: Pediatrics / Volume 12 / October 2013
Fig. 2.  Case 5. Preembolization digital subtraction angiograms of
the lateral left internal carotid artery injection (A), lateral left vertebral
artery injection (B), and superimposed, separate carotid and vertebral
injections (C) showing a left parietooccipital PAVF arising from the left
pericallosal and PCA with drainage into the straight sinus and an asso-
ciated venous varix (circle). Embolization was performed through a mi-
crocatheter threaded from the vertebral artery through the PCA across
the fistula and into the distal anterior cerebral artery. Postembolization
angiogram demonstrating obliteration of the PAVF with no filling from
either the internal carotid artery or vertebral artery on separate injec-
tions (circle, D).
(GDCs and NBCA glue) to achieve complete obliteration
of the PAVF.
Notably, there were very few patients (4 [3.5%] of 113)
in the literature review whose PAVFs were embolized with
Onyx, which contrasts with the increasing usage of this
agent for treating other cerebrovascular malformations, es-
pecially in the adult population. At our institution, NBCA
glue is preferred over Onyx, because Onyx utilization typi-
cally extends the embolization29 and requires more fluoro-
scopic time,49 which potentially increases the detrimental
effects of ionizing radiation on children’s developing ner-
vous systems. Furthermore, the potentially large doses of
Onyx required for embolization of these fistulas increas-
es the risk for the rare complication of DMSO (dimethyl
sulfoxide)–related pulmonary toxicity39,46 associated with
Onyx. This pulmonary toxicity may exacerbate the preex-
isting cardiovascular and pulmonary comorbidities often
seen in this group of children.
Complications and Outcomes
Procedure-related death was infrequent in the litera-
ture review (3.0%), representing 4 patients who died of
ICH after embolization.30,40 The most common procedure-
related complication reported in the literature was the de-
velopment of new intracranial hemorrhage occurring in
17 (12.6%) of 135 patients, followed by the development
of new neurological deficit (10 [7.4%] of 135 patients; Ta-
ble 3). Complication rates in series of patients with related
malformations, such as vein of Galen aneurysmal malfor-
mations, have been reported at 17%–36%.19,25,34
Among cases in the literature in which outcome was
347
 P. J. Madsen et al.
TABLE 3: Composite data from a literature review of 147 pediatric TABLE 3: Composite data from a literature review of 147 pediatric
patients presenting with PAVFs* patients presenting with PAVFs* (continued)

Parameter Value Parameter Value

patient demographics (n = 147) complications (n = 135)§,¶ (continued)
 age  seizure 1 (0.7)
  mean 5.02 yrs   mental retardation 1 (0.7)
  range 0 days–17 yrs   glued microcatheter 1 (0.7)
  male/female ratio 1.5:1   pedicle embolization 1 (0.7)
  male 88 (59.9) outcome (n = 130)¶
  female 59 (40.1)   excellent (no deficit) 85 (65.4)
common presenting signs/symptoms (n = 147)   good (minimal deficit) 21 (16.2)
 seizure 36 (24.5)  poor 13 (10.0)
 CHF 28 (19.0)  death 11 (8.5)
  neurological deficit 27 (18.4) average LOF (n = 49)¶ 17.4 mos
 headache 24 (16.3)
 hemorrhage 22 (15.0) *  Unless otherwise noted, values represent the number of patients (%).
DAVF = dural arteriovenous fistula; IVH = intraventricular hemorrhage;
 macrocephaly 21 (14.3)
LOF = length of follow-up; SAH = subarachnoid hemorrhage; SDH =
  genetic syndrome 19 (12.9) subdural hemorrhage; SRS = stereotactic radiosurgery.
  developmental delay 12 (8.2) †  Includes only cases in which the presence or absence of varix was
presence of varix (n = 119)† noted or could be determined from images provided.
 present 110 (92.4) ‡  The sum of individual treatment numbers is greater than the total
 absent 9 (7.6) number of treated patients because some patients had multiple inter-
ventions.
treatment modality (n = 135)‡
§  The sum of individual complications is greater than the total number
  surgical clipping/resection 23 (17.0) of patients with complications because some patients had multiple com-
 embolization 113 (83.7) plications.
  w/ glue 53 (46.9) ¶  Includes only cases in which individual complications, outcomes, or
  w/ coiling 26 (23.0) length of follow-up was reported.
   w/ glue & coiling 21 (18.6)
  balloon occlusion 11 (9.7) clearly reported, the majority of patients (85 [65.4%] of
130) achieved an excellent outcome, defined as the ab-
  Onyx 4 (3.5)
sence of any neurological deficit at follow-up. Twenty-one
  unknown material 2 (1.8) patients (16.2%) were noted to have a minimal neurologi-
 SRS 1 (0.7) cal deficit at follow-up, considered a good outcome, and
 observation 7 (5.2) 13 (10.0%) had a poor outcome, representing a significant
complications (n = 135)§,¶ neurological deficit at follow-up (for example, persistent
 none 102 (75.6) hemiparesis, mental retardation, and persistent visual field
 any 34 (25.2)
deficit). In the literature review, 11 patients died (8.5%);
most deaths were due to either ICH (n = 5) or CHF (n = 4).
  procedure-related death 4 (3.0) The 1 death reported in our series was attributable to the
  any intracranial hemorrhage 17 (12.6) patient’s CHF rather than any neurological compromise.
  ICH 8 (5.9) Patients with a clearly reported outcome in the lit-
  IVH 4 (3.0) erature who presented with ICH had a higher mortality
  SAH 3 (2.2) rate than those without ICH on presentation (4 [18.2%] of
  SDH 2 (1.5)
22 vs 7 [6.5%] of 108, respectively; p = 0.09, Fisher exact
test). In addition to ICH, age at diagnosis also seemed
  new neurological deficit 10 (7.4)
to be a potential indicator of increased mortality. In the
  coil/balloon migration 6 (4.4) reviewed literature the mean age at diagnosis of those pa-
  secondary DAVF 4 (3.0) tients who died was 2.3 ± 3.7 years compared with 5.6 ±
  CSF diversion required 3 (2.2) 5.5 years for those who survived (p = 0.05, unpaired t-
  venous sinus occlusion 3 (2.2) test). The observation of a worse prognosis in younger pa-
  venous infarct 1 (0.7) tients (especially those < 2 years) has also been described
by Hetts et al., who attributed it to the high rate of severe,
 sepsis 1 (0.7)
life-threatening CHF seen in these patients.18 In our lit-
  heart failure 1 (0.7) erature review, 6 (26.1%) of 23 patients with a clear out-
come reported, and who presented with CHF, died, which
(continued)
represents a significantly higher mortality rate compared

348 J Neurosurg: Pediatrics / Volume 12 / October 2013

Pial arteriovenous fistulas in the pediatric population
with the 5 (4.7%) of 107 who died but presented without
CHF symptoms (p = 0.004, Fisher exact test). This find-
ing would support the notion that CHF at presentation is
predictive of a worse prognosis in pediatric patients with
PAVFs.
Our study is limited by the number of cases and its
retrospective nature, which makes it difficult to form
definitive conclusions about the pathogenesis, clinical
course, and optimal treatment strategy for pediatric pa-
tients with PAVF. Our review of the literature is subject to
reporting bias and potentially represents a more historical
perspective rather than a current account of this disease
and its treatment.
Conclusions
This study demonstrates both the serious nature of
PAVF and its heterogeneous presentation. Aggregated
data from the literature suggest that a younger age or pres-
ence of ICH or CHF at presentation may signify a worse
prognosis. Furthermore, older patients seem to present
with more frequent ICH, whereas younger patients pre-
sented significantly more often in CHF. The treatment of
PAVFs has greatly changed with advanced endovascular
techniques. As shown in our series and with a review of
the literature, PAVFs are typically amenable to endovas-
cular intervention; however, they may require more than
one type of embolization material to achieve complete
obliteration. As with many complex medical conditions,
pediatric patients with PAVFs require the input of a team
of physicians in varying disciplines—neurosurgery, inter-
ventional radiology, neurology, and pediatrics—to devel-
op and implement an effective treatment plan.
Disclosure
The authors report no conflict of interest concerning the mate-
rials 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: Heuer, Madsen, Lang,
Storm, Hurst. Acquisition of data: Madsen, Lang, Pisapia, Hurst.
Analysis and interpretation of data: Heuer, Madsen, Lang, Pisapia,
Hurst. Drafting the article: Heuer, Madsen, Lang, Storm, Hurst. Crit-
ically revising the article: all authors. Reviewed submitted version of
manuscript: all authors. Approved the final version of the manuscript
on behalf of all authors: Heuer. Statistical analysis: Madsen, Lang.
Study supervision: Heuer, Storm, Hurst.
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Manuscript submitted March 6, 2013.
Accepted June 20, 2013.
Please include this information when citing this paper: pub-
lished online August 2, 2013; DOI: 10.3171/2013.6.PEDS13110.
Address correspondence to: Gregory G. Heuer, M.D., Ph.D.,
Division of Neurosurgery, The Children’s Hospital of Philadel-
phia, 34th St. & Civic Center Blvd., Philadelphia, PA 19104.
email: Heuerg@email.chop.edu.
J Neurosurg: Pediatrics / Volume 12 / October 2013